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original article
Dispersal spectrum of four forest types along an altitudinal range of the BrazilianAtlantic Rainforest
Valeria Forni Martins1,2,3,5, Lara Priscila Domingues Cazotto4 & Flavio Antonio Maes dos Santos2
1Programa de Pos-graduacao em Ecologia, Institute of Biology, CP 6109, University of Campinas ––
UNICAMP, 13083-970, Campinas, SP, Brazil. www.unicamp.br2Department of Plant Biology, Institute of Biology, CP 6109, University of Campinas –– UNICAMP, 13083-
970, Campinas, SP, Brazil. www.unicamp.br3Current address: Departamento de Ciencias da Natureza, Matematica e Educacao, Centro de Ciencias
Agrarias, CP 153, Universidade Federal de Sao Carlos –– UFSCar, 13600-970, Araras, SP, Brazil. www.cca.
ufscar.br4Graduacao em Ciencias Biologicas, Institute of Biology, CP 6109, University of Campinas –– UNICAMP,
13083-970, Campinas, SP, Brazil. www.unicamp.br5Corresponding author: e-mail: [email protected]
MARTINS, V.F., CAZOTTO, L.P.D., SANTOS, A.M.S. Dispersal spectrum of four forest types along an
altitudinal range of the Brazilian Atlantic Rainforest. http://www.
biotaneotropica.org.br/v14n1/en/abstract?article+bn00614012014
Abstract: In ecological communities, the proportion of plant species with different dispersal syndromes is
known as the dispersal spectrum, which can result from different selective pressures such as climate. This
is because variations in temperature, humidity, atmospheric pressure and precipitation result in distinct
flora and fauna among different sites. If climate conditions along an altitudinal range act as a strong
direct or indirect selective pressure on dispersal syndromes, the dispersal spectrum among plant
communities in different altitudes should be distinct. We organized the dispersal syndromes in five
hierarchical levels according to the levels of detail in diaspore morphology and, consequently, different
degrees of specificity to the dispersers. Then we identified, within each hierarchical level, the syndromes of
tree species of four forest types of the Atlantic Rainforest along a 1200 m altitudinal range in Southeast
Brazil. Among 327 species, we found two syndromes in the most general hierarchical level (abiotic and
biotic dispersal), three in the following level (wind, self and animal), three in the intermediate level
(barochory, autochory and endozoochory), two in the forth level (mammal and bird), and 12 syndromes
in the most specific level, all of which were related to the morphology of diaspores dispersed by wind,
autochory, mammals and birds. The dispersal spectrum in the five hierarchical levels was similar among
the four forest types. Overall, the majority of species is dispersed by biotic agents, considered here as
animals and the parent plant itself. Within biotic agents, the most important are animals, specifically
birds. Most bird-dispersed species present drupoid diaspores. Our results indicate that the selective
pressures on dispersal syndromes originated from climate conditions that vary with altitude are not
strong, hence resulting in the same dispersal spectrum among the forest types.
Keywords: animal dispersal, biotic dispersal, bird dispersal, hierarchy of classification of dispersal
syndromes.
MARTINS, V.F., CAZOTTO, L.P.D., SANTOS, A.M.S. Espectro de dispersao de quatro formacoes
florestais ao longo de um gradiente altitudinal da Mata Atlantica brasileira.
http://www.biotaneotropica.org.br/v14n1/pt/abstract?article+bn00614012014
Resumo: Dentro de uma comunidade, a proporcao de especies vegetais com diferentes sındromes de
dispersao e chamada de espectro de dispersao, o qual pode resultar de distintas pressoes seletivas, como o
clima. Isso ocorre porque variacoes na temperatura, umidade, pressao atmosferica e precipitacao
resultam em flora e fauna distintas entre locais. Assim, podemos esperar que o espectro de dispersao de
comunidades vegetais em diferentes altitudes seja distinto se as condicoes climaticas ao longo do
gradiente altitudinal atuarem como pressao seletiva direta ou indireta sobre as sındromes. Nos
hierarquizamos as sındromes de dispersao em cinco nıveis, de acordo com o detalhamento da morfologia
dos diasporos e, consequentemente, seus diferentes graus de especificidade com os dispersores.
Identificamos, em cada um dos nıveis hierarquicos, as sındromes de especies arboreas de quatro
formacoes florestais da Mata Atlantica ao longo de um gradiente altitudinal de 1200 m no sudeste do
Brasil. Entre 327 especies, encontramos duas sındromes no nıvel hierarquico mais geral (dispersao
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Biota Neotropica. 14(1):e20130003.
abiotica e biotica), tres no nıvel seguinte (vento, propria planta parental e animais), tres no nıvel
intermediario (barocoria, autocoria e endozoocoria), duas no quarto nıvel (mamıferos e aves) e 12
sındromes no nıvel mais especıfico, relacionadas a morfologia dos diasporos dispersos pelo vento,
autocoria, mamıferos e aves. O espectro de dispersao nos cinco nıveis foi similar nas quatro formacoes
florestais. De forma geral, a maior parte das especies e dispersa por agentes bioticos, aqui considerados
animais e a propria planta parental. Dentre os agentes bioticos, os mais importantes sao os animais,
especificamente as aves. A maioria das especies dispersas pelas aves apresenta diasporos drupoides.
Nossos resultados indicam que as pressoes seletivas sobre as sındromes de dispersao ocasionadas pelas
condicoes climaticas que variam com a altitude nao sao fortes. Assim, a ausencia destas pressoes seletivas
resulta em um espectro de dispersao similar entre as formacoes florestais em diferentes altitudes.
Palavras-chave: dispersao biotica, hierarquia de classificacao das sındromes de dispersao, ornitocoria,
zoocoria.
Introduction
Seeds, fruits, infructescences and other dispersal units are
generically called diaspores. Diaspore dispersal is a dynamic
process of diaspore transportation away from the parent plant.
This transportation can be performed by biotic agents, such as
animals and the parent plant itself, or by abiotic agents, such as
wind and water (van der Pijl 1972). Diaspores generally show
adaptations for dispersal by a specific agent (Willson et al.
1990), which is known as dispersal syndrome. Therefore, the
syndromes indicate the most likely primary dispersal agent of a
particular plant species (van der Pijl 1972).
Dispersal syndromes have been extensively described by
Ridley (1930) and van der Pijl (1972). For example, within
biotic dispersal syndromes, animal-dispersed diaspores can be
either fleshy or dry. Many different types of animals consume
the former, which is known as endozoochory; the latter cling
externally to the body of animals, a form of dispersal known as
epizoochory. Endozoochorous diaspores present characteristics
that are specifically attractive to particular groups of animals,
such as ants (although they transport diaspores externally to
their bodies to later remove their fleshy portion inside the nest),
fishes, reptiles, birds or mammals. Conversely, mammal-
dispersed diaspores present characteristics that result in their
dispersal by distinct groups of mammals (Ridley 1930, van der
Pijl 1972). Therefore, there are different levels of detail in
diaspore morphology and, consequently, different degrees of
specificity to the dispersers. In the given example, biotic agents
would be considered level 1 in a hierarchical classification of
dispersal syndromes, as well as abiotic agents; animal dispersal
would be level 2, as well as self dispersal by the parent plant and
the abiotic dispersal by water and wind; endozoochory and
epizoochory would both be level 3, as well as different forms of
self dispersal (autochory and barochory); ant, fish, reptile, bird
and mammal dispersal would all be level 4, and dispersal by the
distinct groups of mammals would be level 5 in the hierarchy,
as well as the different forms of autochory, water and wind
dispersal (for a more detailed explanation of the dispersal
syndromes please see the ‘‘Protocol for the classification of
dispersal syndromes’’ at supplementary material 1).
Despite the clear hierarchical organization of the dispersal
syndromes, no author has yet proposed formal hierarchical
levels within them. This organization is needed in studies that
compare dispersal distances, demographic consequences of
dispersal (e.g., the spatial distribution of seeds and seedlings) or
the proportion of species with different dispersal syndromes in
ecological communities. Restraining diaspore morphology and
consequently its most likely dispersal agent should enable the
evaluation of underlying patterns of dispersal opposed to the
great variation that emerges when syndromes from different
hierarchical levels are considered.
Birds are important dispersal agents, particularly in the
tropics (Gentry 1982, Willson et al. 1989, Pedroni 2001). The
diaspores they eat show very different morphologies, such as
seeds with fleshy appendage, seeds without any nutritional
reward (known as mimetic seeds), and fleshy fruits with few up
to many seeds (i.e. drupoid and baccoid diaspores, respec-
tively). Seeds with fleshy appendages, seeds without any
nutritional reward and seeds from drupoid diaspores are larger
than seeds from baccoid diaspores. Thus, the former may only
be dispersed by large-bodied birds (Wheelwright 1985), which
can swallow the whole diaspore and carry the large seed(s).
Small birds can sometimes swallow large diaspores, but they are
less willing or able to carry the mass of ballast associated with
large seeds (Mack 1993). Therefore, small birds are most likely
to only peck at the pulp of large diaspores and do not act as
dispersers of large seeds. On the other hand, seeds from baccoid
diaspores can be dispersed by both small and large birds, with
the number of seeds carried varying with the size of the bird in
relation to the size of the diaspore, which may be swallowed
whole or have a portion pecked at. Therefore, the different
types of bird-dispersed diaspores are likely to present dissimilar
patterns of seed deposition in the environment as well as
distinct implications for seed germination and establishment of
the new individuals (Howe et al. 1985). Because of the different
selective pressures on each type of bird-dispersed diaspore, it is
necessary to divide them into different groups into level 5 of the
hierarchy of dispersal syndromes.
Even though it is relatively easy to identify seed dispersal
syndromes based on diaspore morphology alone, not necessa-
rily can we predict which agent is actually acting as a disperser.
This is especially critical for animal dispersal, since seed
dispersal mutualisms are clearly unspecialized (Herrera 1985,
2002). Most plants lack attributes that require special handling
by particular species of animals (Herrera 2002, Burns et al.
2009, but see Moran et al. 2004); thus, dispersers rarely show
preferences for particular diaspore traits and often consume
seeds and fruits indiscriminately (e.g., Herrera 1985, Burns et
al. 2009, but see Carlo et al. 2003). Nevertheless, specialized
relationships can arise on coarser taxonomic scales, among
wide ‘guilds’ of diaspores and animals (Lomascolo et al. 2008,
Hollander & Vander Wall 2009, but see Fischer & Chapman
1993). This suggests that the diaspore morphology described in
syndromes belonging to upper levels of the hierarchy proposed
herein can be used with good reliability to predict the set of
dispersal agents of a given plant species. On the other hand,
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biotic syndromes in levels 4 and 5 may hardly correspond to the
actual set of dispersal agents.
This may be considered a shortcoming for the widespread use
of dispersal syndromes, especially the ones in the lower levels of
the hierarchy. Nevertheless, diaspore morphology is likely to
restrict the agents that act as real dispersers, unregard of their
taxonomic group, and these dispersers may deposit seeds in the
environment in similar fashion. For instance, many diaspores with
characteristics considered attractive to birds are also consumed by
mammals. Because seeds belonging to drupoid diaspores are
larger than those belonging to baccoid diaspores, the former are
only likely to be dispersed by large birds and mammals
(Wheelwright 1985), while the latter can be dispersed by both
small and large animals. Large animals have larger home ranges
(Kelt & Van Vuren 2001) and may carry seeds over longer
distances than smaller animals (Seidler & Plotkin 2006). As a
consequence, seeds belonging to drupoid diaspores may be deposit
more scattered in the environment than seeds from baccoid
diaspores, which may show some clumping due to dispersal by
small animals. Hence, diaspores with similar morphology should
be linked to the similar demographic consequences of seed
dispersal, mediated by different dispersal agents. Because of that,
we believe that the biotic syndromes proposed in levels 4 and 5
should be considered in studies of dispersal syndromes.
In ecological communities, the proportion of plant species
with different dispersal syndromes is known as the dispersal
spectrum (van der Pijl 1972, Hughes et al. 1994), which can
result from different selective pressures. The main pressures on
dispersal strategies arise from frugivores (Mazer &
Wheelwright 1993, Lord 2004), predation, competition among
plant species for the same dispersers, climate seasonality and
the environment in which the plants occur (Roth 1987,
Almeida-Neto et al. 2008). Thus, forest types at different
altitudes may have different dispersal spectra due to variations
in temperature, humidity, atmospheric pressure and precipita-
tion (Willson et al. 1990), all of which result in distinct flora and
fauna along an altitudinal range.
The state park ‘‘Parque Estadual da Serra do Mar’’ (PESM
hereafter), Southeast Brazil, is the largest continuous stretch of
preserved Atlantic Rainforest in Brazil and extends from sea
level to 1200 m of altitude (SOS Mata Atlantica/INPE/ISA
1998, Alves et al. 2010). Therefore, it is an excellent site for the
investigation of dispersal spectrum changes with altitude. Both
temperature and rainfall decrease with increasing altitude
(Banco de Dados Climaticos do Brasil), and the different
climate along the altitudinal range has resulted in distinct forest
types, each with its own floristic composition (Joly et al. 2012).
Therefore, we should also expect changes in the dispersal
spectrum along the altitudinal range due to selective pressures
imposed by climate on seed dispersal mechanisms.
As other tropical forests, the Atlantic Rainforest presents
45% up to 90% of shrub and/or tree species dispersed by animals
(Pedroni 2001, Almeida-Neto et al. 2008). Animal dispersal is
positively related to rainfall and hence tends to be more common
at low altitudes (Willson et al. 1989, Vicente et al. 2003).
However, Almeida-Neto et al. (2008) found that animal dispersal
in the Atlantic Rainforest is negatively related to temperature,
which suggests the importance of seed dispersal by animals may
actually increase with increasing altitude. Therefore, the relation
between animal dispersal and altitude should be further explored
in order to depict the relative importance of rainfall and
temperature on the dispersal spectrum.
Within endozoochorous species, bird dispersal is more
common than mammal dispersal (Gentry 1982, Willson et al.
1989). In a 1900 m altitudinal range of the Atlantic Rainforest,
Almeida-Neto et al. (2008) found predominance of bird-
dispersed species at higher altitudes, while mammal-dispersed
species were more frequent at lower altitudes. Last, within
abiotic dispersal, wind and self-dispersed species are more
frequent at higher altitudes, where the climate is drier and
vegetation more open (van der Pijl 1972, Campassi 2006).
Although some studies have shown the influence of climate on
dispersal spectrum changes with altitude, the detailed hier-
archical levels within dispersal syndromes we previously
described have never been taken into account.
This study aimed to (1) develop a hierarchical organization
of dispersal syndromes for tree species, which include four
divisions within bird dispersal based on diaspore morphology,
and (2) identify the syndromes within each hierarchical level for
tree species of four forest types along the altitudinal range of
PESM. After identifying the syndromes, we determined the
dispersal spectrum within each hierarchical level in the four
forest types. Then we specifically asked whether the dispersal
spectrum differed among the forest types.
We expect that dispersal by biotic agents, mainly by animals
that consume diaspores and specifically by birds, should prevail
among tree species at PESM, as found in other studies carried out
in the Brazilian Atlantic Rainforest (e.g., Pedroni 2001, Campassi
2006, Kinoshita et al. 2006, Almeida-Neto et al. 2008, Silva &
Rodal 2009). However, differently from previous studies, the
dispersal spectrum within different hierarchical levels of the
dispersal syndromes will be used, including the divisions within
bird-dispersed diaspores. We hypothesize that, if climate condi-
tions along the altitudinal range of PESM act as a strong selective
pressure on dispersal syndromes, there should be differences in
the dispersal spectrum among the forest types. For example, if
rainfall imposes a stronger pressure, animal dispersal should be
more common at lower altitudes. On the other hand, if
temperature imposes a stronger pressure, animal dispersal should
be more common at higher altitudes. The differences found in the
dispersal spectrum along the altitudinal range should reflect the
key importance of certain dispersal agents in the different
environments, as found by other authors (e.g., van der Pijl
1972, Roth 1987, Willson et al. 1990, Hughes et al. 1994, Pedroni
2001, Campassi 2006, Almeida-Neto et al. 2008).
Material and Methods
1. Study site
The Brazilian Atlantic Forest is considered one of the
world’s hotspots for biodiversity conservation (Myers et al.
2000), with only about 12% of its original cover remaining in
fragments larger than 3 ha (Fundacao SOS Mata Atlantica).
The largest continuous remnant includes the state park PESM
(236349 - 236179 S e 456029 - 456119 W), which encompasses the
mountain range of ‘‘Serra do Mar’’ along the northern coast of
the state of Sao Paulo, SE Brazil. PESM comprises 315,000 ha
(SOS Mata Atlantica/INPE/ISA 1998) ranging from 0 m to
1200 m above sea level (a.s.l.; Alves et al. 2010). The geological
and topological complexity of ‘‘Serra do Mar’’ results in
extremely heterogeneous habitats and microclimates (Suguio &
Martin 1978, Alves et al. 2010), reflected in the different forest
types present at the study site (Alves et al. 2010, Joly et al.
2012).
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In 2006-2007, researchers from the Theme Project
‘‘Functional Gradient’’ (Biota/FAPESP 03/12595-7) installed
14 non-contiguous, permanent 1 ha plots at the four forest types
present along the altitudinal range of PESM. Plot establishment
and tree sampling followed the RAINFOR field manual (Phillips
et al. 2009, Joly et al. 2012). One plot was placed at the Restinga
Forest (up to 10 m a.s.l. in sandy soil; Restinga hereafter), five
plots at the Lowland Atlantic Rainforest (between 5 m and 50 m
a.s.l.; Lowland hereafter), four plots at the Submontane Atlantic
Rainforest (between 50 m and 500 m a.s.l.; Submontane
hereafter) and four plots were installed at the Montane
Atlantic Rainforest (between 500 m and 1200 m a.s.l.; Monane
hereafter; Veloso et al. 2001, Joly et al. 2012). In this study, we
collected data at one plot of each forest type. Because floristic
composition and community structure are very similar among
plots installed at the same forest type (Joly et al. 2012), we believe
the results presented further are representative of the different
forest types of the Atlantic Rainforest at the study site.
At the low portion of ‘‘Serra do Mar’’, mean temperatures
range from 18.46C in July to 25.56C in February. A dry season
is absent and mean rainfall ranges from 11 mm in July to 376
mm in January. At the high portion of ‘‘Serra do Mar’’, mean
temperatures are a little lower and range from 16.46C in July to
23.26C in February. Again, a dry season is absent, but there is
less rainfall than at the low portion of the mountain range (278
mm in February and 20 mm in July; EMBRAPA).
Nevertheless, Submontane and Montane are frequently covered
by clouds and mist brought by oceanic winds (Silva-Dias et al.
1995), which increase humidity but reduce light availability to
plants (Sousa Neto 2008).
Soils along the altitudinal range are shallow and nutrient
poor. However, the soil of Restinga is sandier and poorer than
the soils of the other forest types (Martins 2010). Soil humidity,
total carbon and nitrogen, and ammonia and nitrate concen-
trations increase with altitude. Conversely, decomposition
rates, and N2O and CO2 emissions from the soil to the
atmosphere decrease with altitude (Sousa Neto 2008).
2. Species studied
The researchers from the Theme Project sampled, collected
and identified every living tree (including palms) with stem
DBH > 4.8 cm inside the 14 plots. Voucher specimens are
deposited in the herbariums of the University of Campinas
(UEC), ‘‘Instituto Agronomico de Campinas’’ (IAC) and
‘Universidade Estadual Paulista ‘‘Julio de Mesquita Filho’’’
campus Rio Claro (HRCB; Joly et al. 2012).
We identified the dispersal syndrome within all hierarchical
levels of the species sampled at the four study plots.
Unidentified individuals at the family level and lacking
diaspores in the voucher material were not included in the
analysis. Undetermined species of known families had their
dispersal syndrome assigned when the families had only one
syndrome. Conversely, we were unable to identify the syndrome
of undetermined species belonging to families with more than
one syndrome, except in cases where the diaspores had been
collected. Therefore, the syndrome of undetermined species
with different types of diaspores in the same family was
described as non-identified (NI hereafter).
3. Dispersal syndromes
We conducted a review of the syndromes that occur at tree
species and elaborated a protocol of identification where the
references used can be found (‘‘Protocol for the classification of
dispersal syndromes’’ at supplementary material 1). The
diaspore characteristics presented were extracted from specia-
lized literature rather than based on fruits and seeds of the
species studied. This makes our classification wide enough to be
used by other authors and at other study systems. Based on the
protocol, we also prepared a diagram (Figure 1) that establishes
the hierarchical classification of the dispersal syndromes in five
levels, each composed of several groups.
We created four divisions within bird dispersal based on the
following morphological characteristics: (1) seeds with sarco-
testa, fleshy aril or ariloid structures; (2) seeds with colours that
mimics external fleshy appendages or a juicy aspect; (3) few or
many seeds per diaspore, and (4) size of seeds in relation to the
diaspore. As a result, the divisions created were seeds with
fleshy appendage, seeds without any nutritional reward,
drupoid diaspores and baccoid diaspores (Figure 1).
Diaspores dispersed by mammals present very different
morphologies and are attractive to distinct groups of mammals.
Because of that, syndromes of mammal-dispersed diaspores
originally received their names according to the taxonomic
group of animals that act as the dispersal agent (e.g., Ridley
1930, van der Pijl 1972, Janzen & Martin 1982, Herrera 1989).
However, in the classification here proposed, all other groups
belonging to level 5 were designated based on the morphology
of the diaspores, such as those previously described for bird
dispersal. So, in order for all groups of level 5 to have the same
classification criteria, we proposed new terms for the syn-
dromes of mammal dispersal. The new terms were based on the
main morphological characteristics of the diaspores in each
mammal-dispersed group, which may be related to a taxonomic
group of dispersal agent (Figure 1).
As one can note in Figure 1, some dispersal syndromes are
unfiled to all hierarchical levels. For example, within abiotic
dispersal syndromes (level 1), both wind and water-dispersed
diaspores (level 2) reach a high level of detail without showing
intermediate levels. In the case of wind dispersal, there are dust,
balloon, plumed, winged, ballist and roller diaspores (van der Pijl
1972). We prefer to file them directly to level 5 instead of 3
because they present very specific morphology that, analogously
to biotically dispersed diaspores, enables their classification into
the more detailed level of the hierarchy. The lack of intermediate
levels for abiotic dispersal may suggest that the diversification of
diaspore morphology resulting from selective pressures imposed
by biotic agents is greater than those imposed by abiotic agents.
To identify the dispersal syndromes, we observed the
morphological characteristics of diaspores in the voucher
material deposited in the Herbarium UEC. Since few species
were collected with diaspores, we also used plant images and
drawings, type descriptions in the literature, and/or material
collected outside PESM. Even though diaspores may be
dispersed by animals belonging to different taxonomic groups,
we based our classification on the dispersal syndromes
proposed by Ridley (1930) and van der Pijl (1972), and, more
specifically, on diaspore morphology. Though many species are
subject to secondary dispersal by animals or water, for the
purpose of this study we examined only the primary phase of
dispersal (Seidler & Plotkin 2006).
4. Data analysis
We used chi-square tests to compare the frequency of
occurrence of syndromes within each hierarchical level among
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the four forest types. The expected values for each level were
the total number of species with identified syndromes in the
four forest types together divided by the number of syndromes
within the hierarchical level. We also used chi-square tests to
compare the frequency of occurrence of syndromes within each
hierarchical level in each of the four forest types. The expected
values for level 1 were the total number of species with
identified syndromes divided by two (biotic and abiotic
dispersal). The expected values for further hierarchical levels
were based on the proportion of species belonging to
syndromes from the upper level. For example, for level 2, the
expected values of animal and self dispersal were the number of
biotically dispersed species divided by two, and the expected
values of wind and water dispersal were the number of
abiotically dispersed species divided by two. We did not
perform any comparison among the syndromes of level 3,
because all animal-dispersed species (level 2) presented endo-
zoochorous diaspores (level 3), and the syndromes of
epizoochory, autochory and barochory (all level 3) were
represented by less than five species. For level 5, we performed
chi-square tests for the different types of bird-dispersed
diaspores alone, for the different types of mammal-dispersed
diaspores alone, and for all types of bird, mammal and wind-
dispersed diaspores together. All tests were performed for
categories with sample size of at least five species, with a = 0.05
(Zar 1999).
Results
We listed 83 species at Restinga, 137 at Lowland, 149 at
Submontane and 144 at Montane. Because some species
occurred in more than one forest type, we obtained a final
list with 327 species for the four study plots. Within these
species, one was NI at Restinga (corresponding to 1.2% of the
species in this forest type), three were NI at Lowland (2.2%),
three were undetermined at Montane (2.1%) and 13 were NI at
Figure 1. Diagram with five hierarchical levels of dispersal syndromes. Syndromes in grey boxes are those that definitely do not occur in tree species.For further explanation, please see the ‘‘Protocol for the classification of dispersal syndromes’’ at supplementary material 1.
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Montane (9.0%). The list of all tree species sampled at the four
forest types and their dispersal syndromes belonging to the five
hierarchical levels proposed herein can be found at supplemen-
tary material 2.
As one travels through the diagram that organizes the
hierarchical levels of the dispersal syndromes (Figure 1), the
variation in diaspore morphology and in the group of dispersal
agent decreases from the upper to the lower levels. As a result,
the characteristics of the syndromes become more specific from
the upper to the lower levels.
The frequency of occurrence of dispersal syndromes within
each of the five hierarchical levels did not differ among the four
forest types (P . 0.05; Table 1).The overall dispersal spectrum
of the Atlantic Rainforest at PESM presents more species
dispersed by biotic agents, mainly animals that consume
diaspores and specifically birds, which disperse drupoid
diaspores (Figure 2).
Species were dispersed 6.8 to 15.8 times more by biotic than
by abiotic agents (x2 = 338.10, P , 0.001, d.f. = 3). The
frequency of animal dispersal was higher and that of wind
dispersal lower than expected based on the proportion of
species dispersed by biotic and abiotic agents, respectively (x2 =
244.37, P , 0.001, d.f. = 3). Wind dispersal was the only abiotic
syndrome found in the forest types. Among animal-dispersed
species, bird dispersal was 2.7 to 3.5 times more common than
mammal dispersal (x2 = 117.86, P , 0.001, d.f. = 3; Figure 3).
Within bird dispersal, there was 3.3 to 4 times more drupoid
diaspores than seeds with fleshy appendage attached (x2 =
324.78, P , 0.001, d.f. = 3). Within mammal dispersal, there
was 1.8 to 4.7 times more diaspores with attractive colours
(corresponding to those attractive to primates) than hard
(rodents), clear and opaque (bats), and large diaspores
(Carnivora) together (x2 = 168.17, P , 0.001, d.f. = 3; Table
2). For further explanation on names, please see the ‘‘Protocol
for the classification of dispersal syndromes’’ at supplementary
material 1.
Considering all syndromes of level 5, drupoid diaspores,
diaspores with attractive colours and winged diaspores
occurred at higher frequencies than expected based on the
proportion of bird, mammal and wind-dispersed species
respectively. Seeds with fleshy appendage attached occurred
at a similar frequency to the expected based on the proportion
of bird-dispersed species. Conversely, hard, clear and opaque,
and large diaspores occurred less frequently than expected
based on the proportion of mammal-dispersed species (x2 =
563.81, P , 0.001, d.f. = 12; Table 2).
Discussion
In this study, we propose five hierarchical levels for the
classification of dispersal syndromes based entirely on diaspore
morphology. Using this classification, we found a similar
dispersal spectrum along the altitudinal range of PESM, which
is contrary to the expectation based on previous studies carried
on the Atlantic Rainforest and elsewhere (e.g., van der Pijl
1972, Roth 1987, Willson et al. 1990, Hughes et al. 1994,
Pedroni 2001, Almeida-Neto et al. 2008). Even though climate
is an important determinant of floristic composition along the
altitudinal range (Joly et al. 2012), it probably does not act as a
strong selective pressure on dispersal syndromes, hence result-
ing in the same dispersal spectrum among the forest types.
Alternatively, the selective pressures imposed by rainfall and
temperature may counteract each other and result in a similar
dispersal spectrum along the altitudinal range. Future studies
should also investigate whether the main groups of animal
dispersers change along the altitudinal range, so the dispersal
spectrum can be correlated with the dispersers at the study site.
Almost 90% of tree species at PESM are dispersed by biotic
agents, particularly animals, which is the highest proportion of
animal dispersal described for tropical forests elsewhere
(Pedroni 2001, Kinoshita et al. 2006, Almeida-Neto et al.
2008, Silva & Rodal 2009). This great proportion of animal-
dispersed species at PESM is likely to be related to high rainfall
throughout the year in the mountain range of ‘‘Serra do Mar’’
and the high abundance of vertebrate frugivores in tropical
forests (Gentry 1982, Willson et al. 1989, Vicente et al. 2003,
Almeida-Neto et al. 2008). Most animal-dispersed species at
PESM are attractive to birds, as described in other studies
(Gentry 1982, Willson et al. 1989, Almeida-Neto et al. 2008).
Nevertheless, bird dispersal is 2.7 to 3.5 times more frequent
than mammal dispersal at our study site, which is a much
higher proportion than the previous described 2:1 for the
Neotropics (Gentry 1982, Almeida-Neto et al. 2008). Bird
dispersal is likely to have great implications for seed deposition
patterns and, consequently, for plant demography. This is
because these animals deposit high quantities of seeds in
specific sites (Debussche & Isenmann 1994, Takahashi &
Kamitani 2004), such as near plants with many fruit (Pizo &
Almeida-Neto 2009), taller plants that enable birds to better
visualize both preys and predators (McDonnell 1986,
Debussche & Isenmann 1994), and forest gaps (Debussche &
Isenmann 1994, but also see Loiselle et al. 1996 and Martini &
Santos 2007).
Table 1. Comparisons of the frequency of occurrence of dispersal syndromes within the same hierarchical level (please see Figure 1) among fourforest types of the Atlantic Rainforest in SE Brazil. In all cases, d.f. = 3, except for the last comparison where d.f. = 12.Tabela 1: Comparacoes dafrequencia de ocorrencia das sındromes de dispersao de um mesmo nıvel hierarquico (favor ver Figura 1) entre quatro tipos florestais da MataAtlantica no sudeste do Brasil. Em todos os casos, g.l. = 3, com excecao da ultima comparacao, na qual g.l. = 12.
Syndromes x2 P
Level 1: abiotic agents x biotic agents 4.07 0.25
Level 2: wind x animal 4.05 0.26
Level 4: mammal x bird 0.66 0.88
Level 5: seeds with fleshy appendage attached x drupoid diaspores 0.29 0.96
Level 5: diaspores with attractive colours x (hard ++ clear and opaque ++ large diaspores) 3.15 0.37
Level 5: seeds with fleshy appendage attached x drupoid diaspores x diaspores with attractive
colours x (hard ++ clear and opaque ++ large diaspores) x winged diaspores
4.88 0.18
6 Biota Neotrop
Martins, V.F. et al.
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., 14(1): e20130003, 2014
Most ornithochorous species found at PESM have drupoid
diaspores, which are highly likely to be dispersed by large birds.
The majority of mammal-dispersed species have diaspores
dispersed by primates, which are large animals and can carry
the diaspores distantly from the parent trees (Seidler & Plotkin
2006). Because large animals have larger home ranges (Kelt &
Van Vuren 2001) and may carry seeds over longer distances than
smaller animals (Seidler & Plotkin 2006), the seeds and seedlings
of species dispersed by them can benefit by escaping mortality
due to competition, predation and pathogen infestation near the
parent plant. Conversely, seeds and seedlings can also benefit
from colonization of new habitats (Wang & Smith 2002).
We found low occurrence of species dispersed by wind and
the parent plant itself at PESM. Wind dispersal is predominant
in regions of dry climate (van der Pijl 1972), unlike the Atlantic
Rainforest. Previous studies in this type of forest also found few
species dispersed by the parent plant itself (Vieira et al. 2002).
Possibly, the low frequency of dispersal by wind and the parent
plant itself arises from the low reproductive success of adults
that release their diaspores in dense vegetation where they
cannot travel long distances (Roth 1987). Additionally, the high
diversity of animal dispersers at tropical forests has likely acted
as a selective force driving the evolution of diaspores with
characteristics attractive to animals.
This study shows that there are no differences in the
dispersal spectrum among different forest types along an
altitudinal range in the Atlantic Rainforest at PESM. This
indicates that probably the selective pressures on dispersal
syndromes resulting from climate conditions that vary within
this range are not strong or counteract each other, hence
resulting in the same dispersal spectrum among the forest types.
The high frequency of animal-dispersed species, specifically
bird-dispersed ones, contributes to the same dispersal spectrum
among forest types. The high occurrence of these syndromes
indicates that frugivorous animals, especially birds, are very
important for the maintenance of communities in the Atlantic
Rainforest unregard of altitude.
Acknowledgements
We thank Prof. MSc Jorge Tamashiro and Prof. Dr. Joao
Semir (University of Campinas) for helping with the identifica-
tion of dispersal syndromes; Prof. Dr. Simone Aparecida Vieira
(University of Campinas) and other researchers of the Theme
Project ‘‘Functional Gradient’’ for the species list of each study
site; MSc Larissa Pereira (University of Campinas) for helping
Figure 2. Dispersal spectrum within five hierarchical levels of dispersal syndromes (A – E; please see Figure 1) for the Atlantic Rainforest tree speciesin SE Brazil.
Biota Neotrop 7
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
with the Montane species and voucher specimens; Dr. Lıvia
Cordi (University of Campinas) also for helping with the
voucher specimens; Ataliba Gomes (Instituto Agronomico de
Campinas), Dr. Christiane Correa (University of Campinas), Dr.
Cristina Baldauf (Universidade Federal Rural do Semi-Arido),
Dr. Marco Mello (Universidade Federal de Minas Gerais), Prof.
Dr. Paulo Oliveira and Prof. Dr. Wesley Silva (University of
Campinas) for comments and suggestions; Anne Baldisseri for
English translation of this manuscript; anonymous reviewers for
language correction and valuable suggestions, and Programa de
Pos-Graduacao em Ecologia of the University of Campinas for
financial support. Change the marked text for: This study was
financed by Biota/FAPESP through the Theme Project
Functional Gradient (03/12595-7), by CNPq through a PhD
scholarship (142295/2006-0) and by FAPESP through a post-
doctoral scholarship (2012/00832-0) to VFM, by CNPq through
a scientific initiation scholarship (105612/2009-0) to LPDC, and
by CNPq through a productivity fellowship (1B) to FAMS
(308748/2010-7).
References
ALMEIDA-NETO, M., CAMPASSI, F., GALETTI, M., JORDANO,
P. & OLIVEIRA-FILHO, A. 2008. Vertebrate dispersal syndromes
Figure 3. Percentage of occurrence of dispersal syndromes within four hierarchical levels (A – D; please see Figure 1) for four forest types of theAtlantic Rainforest in SE Brazil.
Table 2. Percentage of occurrence of dispersal syndromes of level 5 (please see Figure 1) for four forest types of the Atlantic Rainforest in SEBrazil. The syndromes of the immediate previous level are given for convenience.Tabela 2: Porcentagem de ocorrencia das sındromes de dispersaodo nıvel 5 (favor ver Figura 1) em quatro tipos florestais da Mata Atlantica no sudeste do Brasil. As sındromes do nıvel imediatamente anterior saodadas por conveniencia.
Dispersal syndromes Forest type
Previous level Level 5 Restinga Lowland Submontane Montane
Bird dispersal Seeds with fleshy appendage attached 14.52 14.02 12.24 15.41
Drupospores 47.83 49.93 49.33 47.56
Baccaspores 7.06 2.16 3.36 2.98
Seeds without any nutritional reward 2.35 0.00 0.67 0.00
Mammal dispersal Hard diaspores 0.00 0.00 0.67 1.19
Diaspores with attractive colours 12.95 15.97 16.96 17.54
Clear and opaque diaspores 5.88 3.59 2.68 6.55
Large diaspores 1.18 0.72 0.67 0.00
Autochory Ballistic release 2.35 1.44 0.67 0.60
Wind dispersal Dust diaspores 0.00 2.88 4.03 1.79
Plumed diaspores 0.00 0.72 0.67 0.00
Winged diaspores 5.88 8.57 8.05 6.38
8 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
., 14(1): e20130003, 2014
along the Atlantic forest: broad-scale patterns and macroecological
correlates. Global Ecol. Biogeogr. 17(4):503-513. doi: http://
dx.doi.org/10.1111/j.1466-8238.2008.00386.x
ALVES, L.F., VIEIRA, S.A., SCARANELLO, M.A., CAMARGO,
P.B., SANTOS, F.A.M., JOLY, C.A. & MARTINELLI, L.A.
2010. Forest structure and abovegroung biomass variation along an
elevational gradient of tropical Atlantic moist forest (Brazil). Forest
Ecol. Manag. 260 (5):679-691. doi: http://dx.doi.org/10.1016/
j.foreco.2010.05.023
BURNS, K.C., CAZETTA, E., GALETTI, M., VALIDO, A. &
SCHAEFER, H.M. 2009. Geographic patterns in fruit colour
diversity: do leaves constrain the colours of fleshy fruits? Oecologia
159(2):337-343. doi: http://dx.doi.org/10.1007/s00442-008-1227-3
CAMPASSI, F. 2006. Padroes geograficos das sındromes de dispersao e
caracterısticas dos frutos de especies arbustivo-arboreas em
comunidades vegetais da Mata Atlantica. Tese de mestrado,
Universidade de Sao Paulo, Escola Superior de Agricultura ‘‘Luiz
de Queiroz’’, Piracicaba.
CARLO, T.A., COLLAZO, J.A. & GROOM, M.J. 2003. Avian fruit
preferences across a Puerto Rican forested landscape: pattern
consistency and implications for seed removal. Oecologia
134(1):119-131. doi: http://dx.doi.org/10.1007/s00442-002-1087-1
DEBUSSCHE, M. & ISENMANN, P. 1994. Bird-dispersed seed rain
and seedling establishment in patchy Mediterranean vegetation.
Oikos 69(3):414-426. doi: http://dx.doi.org/10.2307/3545854
EMBRAPA. http://www.bdclima.cnpm.embrapa.br. Last access in 30/
05/2010.
FISCHER, K.E. & CHAPMAN, C.A. 1993. Frugivores and fruit
syndromes: differences in patterns at the genus and species level.
Oikos 66(3):472-482. doi: http://dx.doi.org/10.2307/3544942
FUNDACAO SOS MATA ATLANTICA. www.sosmatatlantica.org.
br. Last access in 23/04/2011.
GENTRY, A.H. 1982. Patterns of neotropical plant species diversity.
Evol. Biol. 15:1-84. doi: http://dx.doi.org/10.1007/978-1-4615-6968-
8_1
GOMIERO, L.M., SOUZA, U.P. & BRAGA, F.M.S. 2007.
Reproducao e alimentacao de Rhamdia quelen (Quoy & Gaimard,
1824) em rios do Nucleo Santa Virgınia, Parque Estadual da Serra
do Mar, Sao Paulo, SP. Biota Neotrop. 7(3):127-133. http://www.
biotaneotropica.org.br/v7n3/pt/abstract?article++bn01907032007
(last access in 23/07/2013). doi: http://dx.doi.org/10.1590/S1676-
06032007000300015
HERRERA, C.M. 1985. Determinants of plant-animal coevolution: the
case of mutualistic dispersal of seeds by vertebrates. Oikos
44(1):132-144. doi: http://dx.doi.org/10.2307/3544054
HERRERA, C.M. 1989. Frugivory and seed dispersal by carnivorous
mammals, and associated fruit characteristics, in undisturbed
Mediterranean habitats. Oikos 55(2):250-262. doi: http://
dx.doi.org/10.2307/3565429
HERRERA, C.M. 2002. Seed dispersal by vertebrates. In Plant-animal
interactions: an evolutionary approach (C.M. Herrera & O.
Pellmry, ed). Blackwell Scientific Publications, Oxford, p.185-208.
HOLLANDER, J.L. & VANDER WALL, S.B. 2009. Dispersal
syndromes in North American Ephedra. Int. J. Plant Sci.
170(3):323-330. doi: http://dx.doi.org/10.1086/596334
HOWE, H.F., SCHUPP, E.W. & WESTLEY, L.C. 1985. Early
consequences of seed dispersal for a neotropical tree (Virola
surinamensis). Ecology 66(3):781-791. doi: http://dx.doi.org/
10.2307/1940539
HUGHES, L., DUNLOP, M., FRENCH, K., LEISHMAN, M.R., RICE,
B., RODGERSON, L. & WESTOBY, M. 1994. Predicting dispersal
spectra: a minimal set of hypotheses based on plant attributes. J. Ecol.
82(4):933-950. doi: http://dx.doi.org/10.2307/2261456
JANSON, C.H. 1983. Adaptation of fruit morphology to dispersal
agents in a neotropical forest. Science 219(4581):187-189. doi:
http://dx.doi.org/10.1126/science.219.4581.187
JANZEN, D.H. & MARTIN, P.S. 1982. Neotropical anachronisms:
the fruits the Gomphotheres ate. Science 215(4528):19-27. doi:
http://dx.doi.org/10.1126/science.215.4528.19
JOLY, C.A., ASSIS, M.A., BERNACCI, L.C., TAMASHIRO, J.Y.,
CAMPOS, M.C.R., GOMES, J.A.M.A., LACERDA, M.S.,
SANTOS, F.A.M., PEDRONI, F., PEREIRA, L.S. ,
PADGURSCHI, M.C.G., PRATA, E.M., RAMOS, E.,
TORRES, R.B., ROCHELLE, A., MARTINS, F.R., ALVES,
L.F., VIEIRA, S.A., MARTINELLI, L.A., CAMARGO, P.B.C.,
AIDAR, M.P.M., EISENLOHR, P.V., SIMOES, E., VILLANI,
J.P. & BELINELLO, R. 2012. Florıstica e fitossociologia em
parcelas permanentes da Mata Atlantica do sudeste do Brasil ao
longo de um gradiente altitudinal. Biota Neotrop. 12(1):123-145.
http://www.biotaneotropica.org.br/v12n1/en/abstract?arti-
cle++bn01812012012 (last access in 23/07/2013). doi: http://
dx.doi.org/10.1590/S1676-06032012000100012
KELT, D.A. & VAN VUREN, D.H. 2001. The ecology and
macroecology of mammalian home range area. Am. Nat.
157(6):637-645. doi: http://dx.doi.org/10.1086/320621
KINOSHITA, L.S., TORRES, R.B., FORNI-MARTINS, E.R.,
SPINELLI, T., AHN, Y.J. & CONSTANCIO, S.S. 2006.
Composicao florıstica e sındromes de polinizacao e de dispersao
da mata do Sıtio Sao Francisco, Campinas, SP, Brasil. Acta Bot.
Bras. 20(2):313-327. doi: http://dx.doi.org/10.1590/S0102-
33062006000200007
LOISELLE, B.A., RIBBENS, E. & VARGAS, O. 1996. Spatial and
temporal variation of seed rain in a Tropical Lowland Wet Forest.
Biotropica 28(1):82-95. doi: http://dx.doi.org/10.2307/2388773
LOMASCOLO, S.B., SPERANZA, P. & KIMBALL, R.T. 2008.
Correlated evolution of fig size and color supports the dispersal
syndromes hypothesis. Oecologia 156(4):783-796. doi: http://
dx.doi.org/10.1007/s00442-008-1023-0
LORD, J.M. 2004. Frugivore gape size and the evolution of fruit size
and shape in southern hemisphere floras. Austral Ecol. 29(4):430-
436. doi: http://dx.doi.org/10.1111/j.1442-9993.2004.01382.x
MACK, A.L. 1993. The sizes of vertebrate-dispersed fruits: a
neotropical-palaeotropical comparison. Am. Nat. 142(5):840-585.
doi: http://dx.doi.org/10.1086/285575
MARTINI, A.M.Z. & SANTOS, F.A.M. 2007. Effects of distinct types
of disturbance on seed rain in the Atlantic forest of NE Brazil.
Plant Ecol. 190(1):81-95. doi: http://dx.doi.org/10.1007/s11258-006-
9192-6
MARTINS, S.C. 2010. Perdas de nitrogenio pela emissao de oxido
nitroso (N2O) e sua relacao com a decomposicao da serapilheira e
biomassa de raızes na floresta de Mata Atlantica. Tese de
doutorado, Universidade de Sao Paulo, Piracicaba.
MAZER, S.J. & WHEELWRIGHT, N.T. 1993. Fruit size and shape:
allometry at different taxonomic levels in bird-dispersed plants.
Evol. Ecol. 7(6):556-575. doi: http://dx.doi.org/10.1007/
BF01237821
MCDONNELL, M.J. 1986. Old field vegetation height and the
dispersal pattern of bird-disseminated woody plants. B. Torrey
Bot. Club 113(1):6-11. doi: http://dx.doi.org/10.2307/2996227
MORAN, C., CATTERALL, C.P., GREEN, R.J. & OLSEN, M.F.
2004. Functional variation among frugivorous birds: implications
for rainforest seed dispersal in a fragmented subtropical landscape.
Oecologia 141(4):584-595. doi: http://dx.doi.org/10.1007/s00442-
004-1685-1
MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G.,
FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for
conservation priorities. Nature 403(6772):852-858. doi: http://
dx.doi.org/10.1038/35002501
PEDRONI, F. 2001. Aspectos da estrutura e dinamica da comunidade
arborea na Mata Atlantica de planıcie e encosta em Picinguaba,
Ubatuba, SP. Tese de doutorado, Universidade Estadual de
Campinas, Campinas.
Biota Neotrop 9
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
PHILLIPS, O., BAKER, T., FELDPAUSCH, T. & BRIENEN, R.
2009. RAINFOR field manual for plot establishment and
remeasurement. http://www.rainfor.org/en/manuals. Last access in
27/11/2013.
PIZO, M.A. & ALMEIDA-NETO, M. 2009. Determinants of fruit
removal in Geonoma pauciflora, an understorey palm of neotropical
forests. Ecol. Res. 24(6):1179-1186. doi: http://dx.doi.org/10.1007/
s11284-009-0599-0
RIDLEY, H.N. 1930. The dispersal of plants throughout the world. L.
Reeve & CO., LTD., Ashford.
ROTH, I. 1987. Stratification of a tropical forest as seen in dispersal
types. Dr. W. Junk Publishers, Dordrecht.
SEIDLER, T. & PLOTKIN, J.B. 2006. Seed dispersal and spatial
pattern in tropical trees. PLOS Biol. 4(11):2132-2137. doi: http://
dx.doi.org/10.1371/journal.pbio.0040344
SILVA, M.C.N.A. & RODAL, M.J.N. 2009. Padroes das sındromes de
dispersao de plantas em areas com diferentes graus de pluviosidade,
PE, Brasil. Acta Bot. Bras. 23(4):1040-1047. doi: http://dx.doi.org/
10.1590/S0102-33062009000400014
SILVA-DIAS, M.A.E., VIDALE, P.E. & BLANCO, C.M.R. 1995.
Case study and numerical simulation of the summer regional
circulation in Sao Paulo, Brazil. Bound.-Lay. Meteorol. 74(4):371-
388. doi: http://dx.doi.org/10.1007/BF00712378
SOS MATA ATLANTICA/INPE/ISA. 1998. Atlas da evolucao dos
remanescentes florestais e ecossistemas associados ao domınio da
Mata Atlantica no perıodo 1990––95. SOS Mata Atlantica/INPE/
ISA, Sao Paulo.
SOUSA NETO, E.R. 2008. Perdas de nitrogenio pela emissao de oxido
nitroso (N2O) e sua relacao com a decomposicao da serapilheira e
biomassa de raızes na floresta de Mata Atlantica. Tese de mestrado,
Universidade de Sao Paulo, Piracicaba.
SUGUIO, K. & MARTIN, L. 1978. Quaternary marine formations of
the states of Sao Paulo and southern Rio de Janeiro. In
International Symposium on Coastal Evolution in the
Quaternary. Universidade de Sao Paulo, Sao Paulo, p. 55.
TAKAHASHI, K. & KAMITANI, T. 2004. Factors affecting seed rain
beneath fleshy-fruited plants. Plant Ecol. 174(2):247-256. doi:
http://dx.doi.org/10.1023/B:VEGE.0000049105.30878.25
VAN DER PIJL, L. 1972. Principles of dispersal in higher plants. 2 ed.
Springer-Verlag, Wurzburg.
VELOSO, H.P., RANGEL-FILHO, A.L.R. & LIMA, J.C.A. 2001.
Classificacao da vegetacao brasileira, adaptada a um sistema
universal. IBGE, Rio de Janeiro.
VICENTE, A., SANTOS, A.M.M. & TABARELLI, M. 2003. Variacao
no modo de dispersao de especies lenhosas em um gradient de
precipitacao em em floresta seca e umida no nordeste do Brasil. In
Ecologia e conservacao da caatinga (I. Leal, M. Tabarelli & J.M.C.
Silva, ed). Editora Universitaria da UFPE, Recife, p.201-231.
VIEIRA, D.L.M., AQUINO, F.G., BRITO, M.A., FERNANDES-
BULHAO, C. & HENRIQUES, R.P.B. 2002. Sındromes de
dispersao de especies arbustivo-arboreas em cerrado sensu stricto
do Brasil Central e savanas amazonicas. Rev. Bras. Bot. 25(2):215-
220. doi: http://dx.doi.org/10.1590/S0100-84042002000200009
WANG, B.C. & SMITH, T.B. 2002. Closing the seed dispersal loop.
Trends Ecol. Evol. 17(8):379-385. doi: http://dx.doi.org/10.1016/
S0169-5347(02)02541-7
WHEELWRIGHT, N.T. 1985. Fruit size, gape width, and the diets of
fruit-eating birds. Ecology 66(3):808-818. doi: http://dx.doi.org/
10.2307/1940542
WILLSON, M.F., IRVINE, A.K. & WALSH, N.G. 1989. Vertebrate
dispersal syndromes in some Australian and New Zealand plant
communities, with geographic comparisons. Biotropica 21(2):133-
147. doi: http://dx.doi.org/10.2307/2388704
WILLSON, M.F., RICE, B.L. & WESTOBY, M. 1990. Seed dispersal
spectra: a comparison of temperate plant communities. J. Veg. Sci.
1(4):547-562. doi: http://dx.doi.org/10.2307/3235789
ZAR, J.H. 1999. Biostatistical analysis. 4 ed. Prentice-Hall, Upper
Saddle River.
Supplementary material 1: Protocol for the classifi-cation of dispersal syndromes
This protocol includes a description of diaspore and
vegetative characteristics that will help to identify all forms of
diaspore dispersal. The exception are the following forms that
are absent from tree species or that do not present common
traits that indicate a dispersal syndrome: (1) dispersal by slugs,
which does not constitute a dispersal syndrome (Gervais et al.
1998, Tuerke et al. 2010); (2) dispersal by earthworms, which
also does not constitute a dispersal syndrome (Milcu et al.
2006); (3) dispersal by bees, described for only two tree species
with fruits that produce resin or wax (Wallace & Trueman
1995, Wallace et al. 2008); (4) dispersal by beetles, mainly
described for dung beetles, which collect faeces containing seeds
primarily dispersed by vertebrates (Vulinec 2002). However,
beetles have also been found ingesting fruit pulp with seeds of
one parasitic species in the Mediterranean region (de Vega et al.
2011); (5) dispersal by weta, giant flightless crickets in New
Zealand (Burns 2006, Duthie et al. 2006); (6) ant-dispersed
species that form ant gardens and only occur in epiphytes (Ule
1905 apud van der Pijl 1972, van der Pijl 1972); (7) ant-dispersed
species with short stems that droop to the ground when the
seeds are ripe, which can only occur in herbaceous plants
(Handel & Beattie 1990); (8) dispersal by tree-frogs, found only
in a single bromeliad species (Silva et al. 1989); (9) woody or
dry fruits with small hard seeds produced by herbaceous plants;
(10) tumbleweeds, restricted to herbaceous plants, and (11)
diaspores that submerge in water, which only occur in aquatic
species (van der Pijl 1972). The main studies reviewed for the
elaboration of this protocol were: Ridley (1930), van der Pijl
(1972), Roth (1987), Herrera (1989), Banack (1998), Laubhann
& Puff (2002) and Dumont (2003). All characteristics described
here can be observed in herbarium specimens, photographs,
diagrams and information about the species in the literature.
The protocol is organized into hierarchical levels, according
to the diagram in Fig. 1 presented in the paper. The diagram
establishes a hierarchical classification of the dispersal syn-
dromes in five levels, each composed of several groups. At each
subsequent level of the hierarchy, the morphological character-
istics of the diaspores are given in greater detail, thus further
specifying the disperser agents. As a result, the characteristics of
the syndromes become more specific from the upper levels to
the lower levels. Nevertheless, some dispersal syndromes are
unfiled to all hierarchical levels. This happens because some
diaspores reach a high level of detail without showing
intermediate levels and, thus, are classified directly into level
5 of the hierarchy.
A list of all tree species sampled at four forest types of the
Atlantic Rainforest in Southeast Brazil and their dispersal
syndromes belonging to the five hierarchical levels proposed
herein can be found at supplementary material 2. In this
protocol, we only give examples of species with dispersal
syndromes that were not found at the study site.
1. Level 1: Dispersal by biotic agents
1.1. Level 2: Animal dispersal: animal-dispersed diaspores
can either be consumed or stick externally to the body of
animals (Ridley 1930, van der Pijl 1972).
1.1.1. Level 3: Endozoochory (diaspores consumed by
animals): endozoochorous diaspores usually contain a fleshy
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portion, such as fruits with pulp and seeds with fleshy
appendages attached. This fleshy portion primarily provides
nutrients and energy to the animals (Ridley 1930, van der Pijl
1972, Holldobler & Wilson 1990). The diaspores can present
odour, attractive colours (bright yellow, orange, red, pink,
purple, blue or black) and protection against premature
consumption, such as green colour and unpalatable substances
(van der Pijl 1972). The fruits may have hard or soft skin
(Banack 1998, Dumont 2003), and a sweet flavour because,
when ripe, their sugar content increases. Moreover, they
become softer due to the presence of pectin (Raven 2007).
1.1.1.1. Level 4: Ant dispersal: the characteristic diagnosing
this syndrome are seeds covered by an oleaginous external
portion, which generally makes up the elaiosome. The lipid
compounds are volatile and attract ants, which carry the seeds
to their nest to feed on the oleaginous portion, eventually
dispersing the seeds (Ridley 1930, van der Pijl 1972, Holldobler
& Wilson 1990). The groups of ant dispersal presented below
are intended only to facilitate the identification of diaspores
dispersed by ants and are not an actual level within the
syndrome. One example of species dispersed by ants is Mabea
fistulifera Mart.
i- Seeds with elaiosome attached: are characterized by the
presence of a fleshy appendage externally to the seed. It is rich
in lipids and is called the elaiosome (van der Pijl 1972,
Holldobler & Wilson 1990). It is usually white, contrasting with
the seed, which is dark, hard, smooth and apparently difficult
to destroy (van der Pijl 1972). One example of species that
produce seeds with an elaiosome attached is Mabea fistulifera.
ii- Seeds that secrete lipids by the testa: are characterized by
the presence of an oleaginous material distributed throughout
the whole fleshy testa. Sometimes, this material can be found in
small parts of the inflorescence that remain attached to the
seeds (Ridley 1930, van der Pijl 1972). Species of Ficus secrete
lipids by the testa, but we classified the five species of this genus
found in the forest types studied as mammal-dispersed, with
clear and opaque diaspores (correspondent to those attractive
to bats; item 1.1.1.5.3.) because they presented more character-
istics of this syndrome than of ant dispersal.
When the seed has no elaiosome attached or oleaginous
material distributed throughout its fleshy testa, characteristics
of the parent plant may indicate the occurrence of dispersal by
ants. In this case, the plants can facilitate the encounter of the
diaspores by ants, and also provide food and/or shelter for
them. Therefore, while foraging on the plant, the ants find the
diaspores and take them to their nests (Ridley 1930, van der Pijl
1972, Handel & Beattie 1990). The characteristics of the parent
plants indicating the occurrence of dispersal by ants are:
iii- Form of diaspore presentation: dehiscent fruits (open
spontaneously during maturation) that remain open for a long
time and infructescences with seeds that are easily accessible
(Handel & Beattie 1990, Goncalves & Lorenzi 2007). A
herbaceous species with the latter form of presentation of its
diaspores is Urera baccifera (L.) Gaudich. ex Wedd.
iv- Plants with extra-floral nectaries (EFNs) or post-floral
nectaries (PFNs): nectaries are glands that produce nectar, a
secretion rich in sugars. EFNs are usually located on the stem,
the petiole or the leaf blade (van der Pijl 1972, Holldobler &
Wilson 1990, Goncalves & Lorenzi 2007). The PFNs are
located next to the fruits and secrete nectar even during fruit
development (van der Pijl 1972, Ferri et al. 1981). One example
of species with EFNs is Acacia pycnantha Benth.
v- Plants with formicaries: formicaries are spaces in the leaf
or on the stem that serve as shelter for ants (Holldobler &
Wilson 1990). A herbaceous species with formicaries is Tococa
formicaria Mart..
vi- Plants with food bodies: food bodies are small, pearl-like
epidermal structures, showing basal constriction. Lipids and
glycogen are the major metabolites of these structures, which
may be associated with EFNs and formicaries. The food bodies
are located in different parts of the plant, such as in the rachis
(main vein of compound leaves) and pinnule (last leaflets of
leaves with blades divided close to the main vein), or at the base
of the petiole (Ferri et al. 1981, Goncalves & Lorenzi 2007).
One example of species that have food bodies are those
belonging to Acacia.
1.1.1.2. Level 4: Fish dispersal: occurs in species that grow
on riverbanks or in flooded sites. Their diaspores are heavy and
fall off the parent plant into the water where they may either
sink or float. These diaspores may have hard skin, which can
only be opened by the jaws of fish, and many small, hard seeds,
which are not damaged during the passage through the
digestive tract (van der Pijl 1972, Kubitzki & Ziburski 1994).
One example of species dispersed by fish is Eugenia inundata
DC.
1.1.1.3. Level 4: Reptile dispersal (performed by lizards,
alligators and turtles): is characterized by fruits equipped with
odour (van der Pijl 1972), usually with a red or orange colour
(Klimstra & Newsome 1960), and that develop close to the
ground or fall off from the parent plant when ripe. Some species
have fruits equipped with hard skin (van der Pijl 1972). One
example of species dispersed by reptiles is Celtis australis L.
1.1.1.4. Level 4: Bird dispersal: diaspores dispersed by birds
are bright and show contrasting colours, such as red and black,
orange and black, and black or dark blue with light colours;
contrast between the diaspores and leaves; contrast between the
diaspores and its coloured auxiliary organs. The diaspores
usually have an edible part, such as the fruit pulp or fleshy
appendages attached to the seed. However, there are some bird-
dispersed seeds that do not have an edible part, although their
colour is attractive to birds and resembles seeds with fleshy
appendages or fleshy fruits. These seeds are commonly referred
to as mimetic (van der Pijl 1972, Laubhann & Puff 2002),
although there are other hypotheses for the evolution of such
colour pattern (see Peres & van Rossmalen 1996, Foster &
Delay 1998 and Galetti 2002). When immature, bird-dispersed
diaspores have an external protection against premature
consumption; the seeds also have a protection from premature
digestion (van der Pijl 1972). The diaspores are easily accessible
to birds, such as hanging fruit and/or seeds (van der Pijl 1972,
Roth 1987), rarely have an odour (van der Pijl 1972) and are
small (# 2 cm; Willson et al. 1989). Due to the great variation
of bird-dispersed diaspores, they can be classified according to
their morphology into the following groups:
1.1.1.4.1. Level 5: Seeds with fleshy appendage attached: are
characterized by seeds fully or partially covered by sarcotesta,
aril or ariloid structures (Barroso et al. 1999). These
appendages provide a contrasting colour with the seed. The
seeds are exposed in hard-skinned dehiscent fruits (van der Pijl
1972, Laubhann & Puff 2002).
1.1.1.4.2. Level 5: Drupoid diaspores: are characterized by
diaspores with a single or just a few seeds (the species analysed
showed up to six), which are large in relation to the diaspore.
The exocarp, or skin of the fruit or fruitlet, has attractive
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colours to birds and is not rigid. Drupoid diaspores are
indehiscent (do not open during maturation; Goncalves &
Lorenzi 2007). During the dispersal event, mainly large-bodied
birds can swallow the whole diaspore and carry its large seeds
(Wheelwright 1985). Small birds can sometimes swallow
diaspores with a single or just a few large seeds, but they are
less willing or able to carry the mass of ballast associated with
them (Mack 1993). Therefore, small birds are most likely to
only peck at the pulp of drupoid diaspores and do not act as
dispersers of their large seeds.
1.1.1.4.3. Level 5: Baccoid diaspores: are characterized by
diaspores with dozens or hundreds of small seeds immersed in
the pulp. The exocarp has attractive colours to birds and is not
rigid. Baccoid diaspores are indehiscent. During the dispersal
event, a bird carries several seeds belonging to the same baccoid
diaspore: the number of seeds varies with the size of the bird in
relation to the size of the diaspore, which may be swallowed
whole or have a portion pecked at. The terms drupoid and
baccoid diaspores were here employed because, even though
there are classifications for fruits in the literature, there are no
specific terms for diaspores (either a single fruit, or a fruitlet
from a compound fruit or infructescence) with these character-
istics.
1.1.1.4.4. Level 5: Seeds without any nutritional reward: are
characterized by seeds with colours similar to that of seeds with
a fleshy appendage so that they appear to have one. Seeds
without nutritional reward may also appear to be juicy, similar
to a fleshy fruit. However, they are hard and dry (van der Pijl
1972, Laubhann & Puff 2002).
1.1.1.5. Level 4: Mammal dispersal: the diaspores are usually
large (. 2 cm; Ridley 1930, van der Pijl 1972) and the seeds are
protected from premature digestion. Some fruits have an
external protection against premature consumption, while the
edible portion in others has a green colour even when ripe. The
ripe fruits may have a strong odour, which is typical of
diaspores dispersed by mammals (van der Pijl 1972). Mammal-
dispersed fruits have a watery pulp (van der Pijl 1972,
Albuquerque 2001) and hard or soft skin (Banack 1998,
Dumont 2003), lie outside the foliage attached to the stem or
near the ground, and fall off the parent plant continuously.
Attractive colours are not always present (van der Pijl 1972).
Mammals can also disperse dry fruits, or consume large seeds
with yellow or orange fleshy appendages. Due to the great
variation of mammal-dispersed diaspores, they can be classified
according to their morphology into the following groups:
1.1.1.5.1. Level 5: Hard diaspores (attractive to rodents): are
often equipped with a hard exocarp (van der Pijl 1972), green
pericarp and one or more seeds (Ridley 1930). The typical
odour found in mammal-dispersed fruits is absent (van der Pijl
1972). Some fruits belonging to this group are fleshy, made up
of red, green or yellow capsules, with seeds surrounded by a
white pulp (Ridley 1930). Seeds with hard, waxy ariloid
structures attached also belong to this group (van der Pijl 1972).
1.1.1.5.2. Level 5: Diaspores with attractive colours (attrac-
tive to primates): are characterized by the most coloured fruits
amongst those dispersed by mammals (van der Pijl 1972), with
black, purple, pink, yellow, orange or grey-green colours
(Ridley 1930). The fruits belonging to this group may have
hard or soft skin, a strong odour (but not a rotten smell) and
juiciness (van der Pijl 1972). Seeds with a yellow or orange aril
(Ridley 1930, van der Pijl 1972), much larger than those
dispersed by birds, also belong to this group (Ridley 1930).
1.1.1.5.3. Level 5: Clear and opaque diaspores (attractive to
bats): are characterized by clear and opaque colours (van der
Pijl 1972), in shades of purple, blue, green, yellow, yellow-
green, white or orange. They contrast with the darker foliage
and make the diaspores more easily seen at night by bats
(Dumont 2003). Clear and opaque diaspores are unprotected
and exposed on branches, generally have a watery pulp (van der
Pijl 1972, Albuquerque 2001) and may be equipped with hard
or soft skin (Banack 1998, Dumont 2003). They often have a
strong odour, conferred by aromatic compounds; the odour is
not necessarily a rotten smell and may be imperceptible to
humans. The fruit shape is highly variable and may be spherical
to cob-shaped (M.A.R. Mello personal communication). The
fruits are of different sizes (Dumont 2003) and occur mainly in
the families Araceae, Clusiaceae, Cucurbitaceae, Moraceae,
Piperaceae, Solanaceae and Urticaceae (van der Pijl 1972,
Mello et al. 2008).
1.1.1.5.4. Level 5: Large diaspores (attractive to mammals
belonging to the order Carnivora): are characterized by fruits
that are much heavier (2.23 g ± 4.05 g) than those dispersed by
birds and other mammals (with the exception of diaspores with
attractive colours and anachronistic fruits), rich in pulp (68.9%
± 18.6% of fresh fruit mass) and with many seeds (60 ± 258
seeds/fruit; Herrera 1989). They also have a specific odour and
commonly fall off the parent plant when ripe. Their colours are
attractive, such as red, black, and mainly brown, white, blue
and green (Ridley 1930, Herrera 1989). The fruits of this group
generally belong to herbaceous plants and to species of
Arecaceae (Ridley 1930, van der Pijl 1972).
1.1.1.5.5. Level 5: Anachronistic fruits: are characterized by
very large, indehiscent fruits (much larger than those belonging
to the other syndromes) with a pulp rich in oil, sugar or
nitrogen compounds. They lack any attractive colour. The
hardness, size and weight of these fruits are similar to those
consumed by large African mammals. These features indicate
that the anachronistic fruits were dispersed by the South
American megafauna, which became extinct about 10,000 years
ago. After the extinction of these animals, there might have
been a population decline of the plant species dispersed by
them, although some would still remain viable due to sporadic
dispersal by other agents (Janzen & Martin 1982, Guimaraes Jr.
et al. 2008). Other characteristics of anachronistic fruits are the
presence of seeds enclosed within a hard or thick endocarp, or
soft or fragile seeds that are very small or embedded in a hard
portion of the fruit (Janzen & Martin 1982). Examples of
species of this group are: Crescentia alata Kunth, Enterolobium
cyclocarpum (Jacq.) Griseb. and Hippomane mancinella L.
1.1.2. Level 3: Epizoochory (or exozoochory; diaspores that
cling externally to the body of animals): the diaspores do not
have an edible portion and therefore do not provide resources
for animals. They also do not have attractive colours and
odour, and have a rough texture (Sorensen 1986) and adhering
mechanisms such as thorns, barbs, hairs (usually hard and
curved), hooks or sticky exudates (van der Pijl 1972, Sorensen
1986, Raven 2007) which allow the diaspores to stick to animal
scales, feathers and fur. The diaspores may be dry fruits that are
easily detached from the parent plant when ripe. They develop
near the ground and occur mainly in herbaceous species (Ridley
1930, van der Pijl 1972). Examples of herbaceous epizoochor-
ous species are: Acanthospermum hispidum DC., Bidens laevis
(L.) B.S.P. and Desmodium psilophyllum Schlecht.; we did not
find any example of a tree species with this syndrome.
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1.2. Level 2: Self dispersal (dispersal performed by the
parent plant itself):
1.2.1. Level 3: Autochory (dispersal performed actively by
the parent plant): is characterized by diaspores with brown or
pale colours (Roth 1987). Autochorous diaspores can be
released from the parent plant in two ways:
1.2.1.1. Level 5: Explosive or ballistic release: is character-
ized by seeds and fruits with structures or mechanisms (turgor
and hygroscopic movements) that shoot the diaspores away
from the parent plant. They are usually dry fruits (van der Pijl
1972, Albuquerque 2001).
1.2.1.2. Level 5: Blastochory: is characterized by the growth
of branches with fruits at the tip, causing the seeds to fall
further away from the parent plant (van der Pijl 1972).
Examples of herbaceous species of this group are: Aegilops
ovata L. and Erodium ciconium (L.) L’Her.; we did not find any
example of a tree species with blastochorous diaspores.
1.2.2. Level 3: Barochory (fall of the diaspores because of
gravity): is characterized by diaspores with aerodynamic shapes
such as a round one, and a relatively large mass (van der Pijl
1972). Some barochorous species have dry fruits (such as
capsules that open at the sept; Goncalves & Lorenzi 2007),
from which the seeds are detached (Albuquerque 2001).
2. Level 1: Dispersal by abiotic agents
2.1. Level 2: Wind dispersal: is characterized by dry fruits
without attractive colours, which is often brown. The fruits are
equipped with numerous seeds of generally small mass (van der
Pijl 1972). Wind-dispersed diaspores can be classified according
to their morphological characteristics into the following
groups:
2.1.1. Level 5: Dust diaspores: are characterized by very
small and light weighted seeds (about 10-6 g; van der Pijl 1972).
2.1.2. Level 5: Balloons: are characterized by small seeds
with testa in the shape of a balloon, or balloon-shaped fruits
such as inflated and indehiscent pods. Sometimes this shape is
provided by an auxiliary organ such as a bracteole or the
perianth (van der Pijl 1972). One example of species of this
group is Colutea arborescens L.
2.1.3. Level 5: Plumed diaspores: have hairs originated from
different structures. The hairs can be long (single or more than
one) or occur in tufts (van der Pijl 1972). Some plumed seeds
are encased in a capsule or pod and the hairs expand externally
to the fruit. These hairs can be thin, simple, straight and silky;
branched or tangled; or form a woolly mass (Ridley 1930). The
diaspores belonging to this group have well-developed, smooth,
silky hairs, different from the hard ones of epizoochorous
diaspores (Sorensen 1986).
2.1.4. Level 5: Winged diaspores: are characterized by one or
more flattened protrusions called wings, which may originate
from the seed, the fruit or auxiliary organs (van der Pijl 1972).
2.1.5. Level 5: Wind-ballists (anemoballists): are character-
ized by diaspores that are released explosively after a gust of
wind. They are heavier than wind-dispersed diaspores belong-
ing to the other groups (van der Pijl 1972). One herbaceous
species of this group is Papaver somniferum L.; we did not find
any example of a tree species dispersed ballistically by wind.
2.2. Level 2: Water dispersal: occurs mainly in plants from
aquatic environments (Ridley 1930, van der Pijl 1972), but has
also been described for a herbaceous species in the Atlantic
Rainforest (Pizo & Morellato 2002). The diaspores can often
float, at least for short distances, and are heavier than those
dispersed by wind (Ridley 1930, van der Pijl 1972). One
example of a species dispersed by water is Cocos nucifera L.
Water-dispersed diaspores can be classified according to their
morphological characteristics into the following groups:
2.2.1. Level 5: Rain wash (ombrohydrochory): is character-
ized by brown coloured dry fruits equipped with numerous
seeds, as in some wind-dispersed diaspores. However, they are
heavier than the latter (van der Pijl 1972). Examples of
herbaceous species of this group are: Geigeria acaulis (Sch.
Bip.) Benth & Hook. Ex Oliv. & Hiern., Leptaleum filifolium
(Willd.) DC. and Sedum acre L.; we did not find any example of
a tree species with rain wash dispersal.
2.2.2. Level 5: Rain-ballists: are characterized by seeds that
are released explosively from the fruit driven by rainfall. The
seeds are released from cup-shaped fruits, by a catapult
mechanism of the fruit or through fruit pores (van der Pijl
1972, Pizo & Morellato 2002). The latter was described for
Bertolonia mosenii Cogn. (Melastomataceae), a perennial herb of
the Atlantic Rainforest: the rainfall squeezes the seeds out of the
triangular capsule-fruit through pores present at its vertices
(known as the squirt-corner mechanism). The seeds are obovate
(oval-shaped, with a wider part toward the apex of the seed) and
cleaved (club-shaped, with a dilated portion on the extremities;
Ferri et al. 1981, Pizo & Morellato 2002), contrasting with the
seeds released from cup-shaped fruits, which are lenticular (lens-
shaped; Pizo & Morellato 2002). Examples of herbaceous species
of this group are: Bertolonia mosenii, Ocimum basilucum L. and
Thlaspi perfoliatum L.; we did not find any example of a tree
species dispersed ballistically by rain.
2.2.3. Level 5: Floating diaspores: are generally seeds that
have both a waterproof testa and low density, which is possible
due to the presence of aerenchyma, light albumen and
cotyledons, or corky tissues (van der Pijl 1972). Examples of
species of this group are: Cocos nucifera and Hevea brasiliensis
(Willd. ex Adr. de Juss.) Muell-Arg.
Diaspores without specific morphological characteristics: are
characterized by the absence of morphological features that
allow us to identify the syndrome to which they belong.
References
ALBUQUERQUE, L.B. 2001. Polinizacao e dispersao de sementes em
Solanaceas Neotropicais. Tese de doutorado, Universidade
Estadual de Campinas, Campinas.
BANACK, S.A. 1998. Diet selection and resource use by flying foxes
(genus Pteropus). Ecology 79(6):1949-1967. doi: http://dx.doi.org/
10.1890/0012-9658(1998)079[1949:DSARUB]2.0.CO;2
BARROSO, G.M., MORIM, M.P., PEIXOTO, A.L. & ICHASO,
C.L.F. 1999. Frutos e sementes, morfologia aplicada a sistematica
de dicotiledoneas. Editora da Universidade Federal de Vicosa,
Vicosa.
BURNS, K.C. 2006. Weta and the evolution of fleshy fruits in New
Zealand. New Zeal. J. Ecol. 30(3):405-406.
DE VEGA, C, ARISTA, M., ORTIZ, P.L., HERRERA, C. M. &
TALAVERA, S. 2011. Endozoochory by beetles: a novel seed
dispersal mechanism. Ann. Bot. 107(4):629-637. doi: http://
dx.doi.org/10.1093/aob/mcr013
DUMONT, E. 2003. Bats and fruits: an ecomorphological approach. In
Bat ecology (T.H. Kunz & M.B. Fenton, ed). The University of
Chicago Press, Chicago, p.398-429.
DUTHIE, C., GIBBS, G. & BURNS, K.C. 2006. Seed dispersal by
weta. Science 311(5767):1575. doi: http://dx.doi.org/10.1126/
science.1123544
Biota Neotrop 13
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
FERRI, M.G., MENEZES, N.L. & MONTEIRO, W.R. 1981.
Glossario ilustrado de botanica. Nobel, Sao Paulo.
FOSTER, M.S. & DELAY, L.S. 1998. Dispersal of mimetic seeds of
three species of Ormosia (Leguminosae). J. Trop. Ecol. 14(4):389-
411. doi: http://dx.doi.org/10.1017/S0266467498000303
GALETTI, M. 2002. Seed dispersal of mimetic fruits: parasitism,
mutualism, aposematism or exaptation? In Seed dispersal and
frugivory: ecology, evolution and conservation (D.J. Levey, W.R.
Silva & Galetti, M., ed). CABI Publishing, Cambridge, p.177-191.
GERVAIS, J.A., TRAVESET, A. & WILLSON, M.F. 1998. The
potential of seed dispersal by the Banana Slug (Ariolimax
columbianus). Am. Midl. Nat. 140(1):103-110. doi: http://
dx.doi.org/10.1674/0003-0031(1998)140[0103:TPFSDB]2.0.CO;2
GONCALVES, E.G. & LORENZI, H. 2007. Morfologia vegetal:
organografia e dicionario ilustrado de morfologia das plantas
vasculares. Instituto Plantarum de Estudos da Flora, Nova Odessa.
GUIMARAES JR., P.R.; GALETTI, M. & JORDANO, P. 2008. Seed
dispersal anachronisms: rethinking the fruits extinct megafauna ate.
PLOS One 3(3):e1745. doi: http://dx.doi.org/10.1371/journal.-
pone.0001745
HANDEL, S.N. & BEATTIE, A.J. 1990. Seed dispersal by ants. Sci.
Am. 263(2):76-83. doi: http://dx.doi.org/10.1038/scientificameri-
can0890-76
HERRERA, C.M. 1989. Frugivory and seed dispersal by carnivorous
mammals, and associated fruit characteristics, in undisturbed
Mediterranean habitats. Oikos 55(2):250-262. doi: http://
dx.doi.org/10.2307/3565429
HOLLDOBLER, B. & WILSON, E.O. 1990. The ants. The Belknap
Press, Cambridge.
JANZEN, D.H. & MARTIN, P.S. 1982. Neotropical anachronisms:
the fruits the Gomphotheres ate. Science 215(4528):19-27. doi:
http://dx.doi.org/10.1126/science.215.4528.19
KLIMSTRA, W.D. & NEWSOME, F. 1960. Some observations on the
food coactions of the common Box Turtle (Terrapene c. caroline).
Ecology 41(4):639-647. doi: http://dx.doi.org/10.2307/1931795
KUBITZKI, K. & ZIBURSKI, A. 1994. Seed dispersal in flood plain
forest of Amazonia. Biotropica 26(1):30-43. doi: http://dx.doi.org/
10.2307/2389108
LAUBHANN, D. & PUFF, C. 2002. Birds and bird colors - Flowers
pollinated by birds; diaspores dispersed by birds. Examples from
the flora of Thailand. Botanical Student Field Trip to Thailand
February/March:153-170.
MACK, A.L. 1993. The sizes of vertebrate-dispersed fruits: a
neotropical-palaeotropical comparison. Am. Nat. 142(5):840-585.
doi: http://dx.doi.org/10.1086/285575
MELLO, M.A.R., KALKO, E.K.V. & SILVA, W.R. 2008. Diet and
abundance of the bat Sturnira lilium (Chiroptera) in a Brazilian
Montane Atlantic Forest. J. Mammal. 89(2):485-492. doi: http://
dx.doi.org/10.1644/06-MAMM-A-411R.1
MILCU, A., SCHUMACHER, J. & SCHEU, S. 2006. Earthworms
(Lumbricus terrestris) affect plant seedling recruitment and micro-
habitat heterogeneity. Funct. Ecol. 20(2):261-268. doi: http://
dx.doi.org/10.1111/j.1365-2435.2006.01098.x
PERES, C.A. & VAN ROSSMALEN, M.G.M. 1996. Avian dispersal
of mimetic seeds of Ormosia lignivalvis by terrestrial granivores:
deception or mutualism? Oikos 75(2):249-258. doi: http://
dx.doi.org/10.2307/3546248
PIZO, M.A. & MORELLATO, L.P.C. 2002. A new rain-operated seed
dispersal mechanism in Bertolonia mosenii (Melastomataceae), a
Neotropical rainforest herb. Am. J. Bot. 89(1):169-171. doi: http://
dx.doi.org/10.3732/ajb.89.1.169
RAVEN, P.H., EVERT, R.F. & EICHHORN, S.E. 2007. Biologia
vegetal. 7 ed. Editora Guanabara Koogan, Rio de Janeiro.
RIDLEY, H.N. 1930. The dispersal of plants throughout the world. L.
Reeve & CO., LTD., Ashford.
ROTH, I. 1987. Stratification of a tropical forest as seen in dispersal
types. Dr. W. Junk Publishers, Dordrecht.
SILVA, H.R., BRITO-PEREIRA, M.C. & CARAMASCHI, U. 1989.
Frugivory and seed dispersal by Hyla truncata, a neotropical tree-
frog. Copeia 1989(3):781-783. doi: http://dx.doi.org/10.2307/1445517
SORENSEN, A.E. 1986. Seed dispersal by adhesion. Annu. Rev. Ecol.
Syst. 17(1):443-463. doi: http://dx.doi.org/10.1146/annur-
ev.es.17.110186.002303
TUERKE, M., HEINZE, E., ANDREAS, K., SVENDSEN, S.M.,
GOSSNER, M.M. & WEISSER, W.W. 2010. Seed consumption
and dispersal of ant-dispersed plants by slugs. Oecologia
163(3):681-693. doi: http://dx.doi.org/10.1007/s00442-010-1612-6
VAN DER PIJL, L. 1972. Principles of dispersal in higher plants. 2 ed.
Springer-Verlag, Wurzburg.
VULINEC, K. 2002. Dung beetle communities and seed dispersal in
primary forest and disturbed land in Amazonia. Biotropica
34(2) :297-309. doi : ht tp : / /dx .doi .org /10 .1111/ j .1744-
7429.2002.tb00541.x
WALLACE, H.M. & TRUEMAN, S.J. 1995. Dispersal of Eucalyptus
torelliana seeds by the resin-collecting stingless bee, Trigona
carbonaria. Oecologia 104(1):12-16. doi: http://dx.doi.org/10.1007/
BF00365556
WALLACE, H.M., HOWELL, M.G. & LEE, D.J. 2008. Standard yet
unusual mechanisms of long-distance dispersal: seed dispersal of
Corymbia torelliana by bees. Divers. Distrib. 14(1):87-94. doi:
http://dx.doi.org/10.1111/j.1472-4642.2007.00427.x
WHEELWRIGHT, N.T. 1985. Fruit size, gape width, and the diets of
fruit-eating birds. Ecology 66(3):808-818. doi: http://dx.doi.org/
10.2307/1940542
WILLSON, M.F., IRVINE, A.K. & WALSH, N.G. 1989. Vertebrate
dispersal syndromes in some Australian and New Zealand plant
communities, with geographic comparisons. Biotropica 21(2):133-
147. doi: http://dx.doi.org/10.2307/2388704
14 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
Received: 23/07/2013Revised: 07/01/2014
Accpeted: 26/03/2014
., 14(1): e20130003, 2014
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dro
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Fo
rest
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Gen
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Sp
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evel
5
RA
na
card
iace
ae
Ta
pir
ira
gu
ian
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SA
nn
on
ace
ae
An
no
na
caca
ns
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MA
nn
on
ace
ae
An
no
na
do
lab
rip
eta
laB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
SA
nn
on
ace
ae
An
no
na
seri
cea
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
L,
S,
MA
nn
on
ace
ae
Gu
att
eria
au
stra
lis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RA
nn
on
ace
ae
Gu
att
eria
sp.
4B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SA
po
cyn
ace
ae
Ma
lou
etia
cest
roid
esA
bio
tic
Win
dN
SN
SP
lum
ed
R,
LA
po
cyn
ace
ae
Ta
ber
na
emo
nta
na
laet
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RA
qu
ifo
lia
cea
eIl
exd
um
osa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RA
qu
ifo
lia
cea
eIl
exin
teg
erri
ma
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SA
qu
ifo
lia
cea
eIl
exsp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RA
qu
ifo
lia
cea
eIl
exth
eeza
ns
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SA
rali
ace
ae
Den
dro
pa
na
xcu
nea
tus
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RA
rali
ace
ae
Ore
op
an
ax
cap
ita
tus
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
R,
L,
MA
rali
ace
ae
Sch
effl
era
an
gu
stis
sim
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MA
rali
ace
ae
Sch
effl
era
calv
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
SA
reca
cea
eA
stro
cary
um
acu
leati
ssim
um
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
La
rge
RA
reca
cea
eB
act
ris
seto
saB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
R,
L,
S,
MA
reca
cea
eE
ute
rpe
edu
lis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SA
reca
cea
eS
ya
gru
sp
seu
do
coco
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MA
reca
ceae
Un
det
erm
ined
Bio
tic
An
imal
En
do
zoo
cho
ryN
IN
I
MA
ster
ace
ae
Pip
toca
rph
am
acr
op
od
aA
bio
tic
Win
dN
SN
SW
ing
ed
L,
S,
MA
ster
ace
ae
Ver
no
na
nth
ura
dis
colo
rA
bio
tic
Win
dN
SN
SW
ing
ed
S,
MA
ster
ace
ae
Ver
no
na
nth
ura
pu
ber
ula
Ab
ioti
cW
ind
NS
NS
Win
ged
SB
ign
on
iace
ae
Ha
nd
roa
nth
us
serr
ati
foli
us
Ab
ioti
cW
ind
NS
NS
Win
ged
MB
ign
on
iace
ae
Ja
cara
nd
am
on
tan
aA
bio
tic
Win
dN
SN
SW
ing
ed
RB
ign
on
iace
ae
Ja
cara
nd
ap
ub
eru
laA
bio
tic
Win
dN
SN
SW
ing
ed
L,
MB
ora
gin
ace
ae
Co
rdia
sell
ow
ian
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SB
ora
gin
ace
ae
Co
rdia
tag
ua
hy
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MC
ard
iop
teri
dace
ae
Cit
ron
ella
meg
ap
hy
lla
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SC
ard
iop
teri
dace
ae
Cit
ron
ella
pa
nic
ula
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LC
ari
cace
ae
Ja
cara
tia
spin
osa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
LC
ela
stra
cea
eM
ay
ten
us
ard
isia
efo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
L,
MC
ela
stra
cea
eM
ay
ten
us
go
no
cla
da
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
MC
ela
stra
cea
eM
ay
ten
us
lito
rali
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
SC
ela
stra
cea
eM
ay
ten
us
sp.
2B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
MC
ela
stra
cea
eM
ay
ten
us
sp.
4B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
Continuedonnextpage
Biota Neotrop 15
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
SC
ela
stra
cea
eM
ay
ten
us
ub
atu
ben
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
L,
SC
ela
stra
cea
eS
ala
cia
gra
nd
ifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MC
hlo
ran
tha
cea
eH
edy
osm
um
bra
sili
ense
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
R,
L,
SC
hry
sob
ala
na
cea
eC
ou
epia
ven
osa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
R,
L,
S,
MC
hry
sob
ala
na
cea
eH
irte
lla
heb
ecla
da
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
S,
MC
hry
sob
ala
na
cea
eL
ica
nia
ho
ehn
eiB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
RC
lusi
ace
ae
Ca
lop
hy
llu
mb
rasi
lien
seB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
RC
lusi
ace
ae
Clu
sia
criu
vasu
bsp
.p
arv
iflo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
SC
lusi
ace
ae
Clu
sia
lan
ceo
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
L,
SC
lusi
ace
ae
Ga
rcin
iag
ard
ner
ian
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
RC
lusi
ace
ae
Kie
lmey
era
pet
iola
ris
Ab
ioti
cW
ind
NS
NS
Win
ged
LC
om
bre
tace
ae
Bu
chen
avi
ak
lein
iiB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
SC
om
bre
tace
ae
Ter
min
ali
aja
nu
are
nsi
sA
bio
tic
Win
dN
SN
SW
ing
ed
L,
MD
ich
ap
eta
lace
ae
Ste
ph
an
op
od
ium
estr
elle
nse
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
R,
L,
SE
laeo
carp
ace
ae
Slo
an
eag
uia
nen
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
L,
ME
laeo
carp
ace
ae
Slo
an
eah
irsu
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
LE
ryth
rox
ila
cea
eE
ryth
rox
ylu
msp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
ME
up
ho
rbia
cea
eA
lch
orn
eag
lan
du
losa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
L,
S,
ME
up
ho
rbia
cea
eA
lch
orn
eatr
ipli
ner
via
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
ME
up
ho
rbia
cea
eC
roto
nm
acr
ob
oth
rys
Bio
tic
Sel
fA
uto
cho
ryN
SB
all
isti
c
LE
up
ho
rbia
cea
eE
up
ho
rbia
cea
esp
.B
ioti
cN
IN
IN
IN
I
L,
SE
up
ho
rbia
cea
eM
ab
eap
irir
iB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RE
up
ho
rbia
cea
eM
arg
ari
tari
an
ob
ilis
Bio
tic
Sel
fA
uto
cho
ryN
SB
all
isti
c
LE
up
ho
rbia
cea
eP
au
san
dra
mo
risi
an
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RE
up
ho
rbia
cea
eP
era
gla
bra
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
SE
up
ho
rbia
cea
eS
ap
ium
gla
nd
ulo
sum
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
LE
up
ho
rbia
cea
eT
etro
rch
idiu
mru
bri
ven
ium
Bio
tic
Sel
fA
uto
cho
ryN
SB
all
isti
c
RF
ab
ace
ae
Ab
are
ma
bra
chy
sta
chy
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Wit
ho
ut
rew
ard
R,
SF
ab
ace
ae
An
dir
afr
ax
inif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
RF
ab
ace
ae
Ba
lizi
ap
edic
ella
ris
Ab
ioti
cW
ind
NS
NS
Win
ged
L,
SF
ab
ace
ae
Co
pa
ifer
ala
ng
sdo
rffi
iB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
LF
ab
ace
ae
Co
pa
ifer
atr
ap
ezif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
SF
ab
ace
ae
Da
hls
ted
tia
pin
na
taB
ioti
cS
elf
Au
toch
ory
NS
Ba
llis
tic
LF
ab
ace
ae
Hy
men
aea
cou
rba
ril
va
r.a
ltis
sim
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
R,
L,
SF
ab
ace
ae
Ing
aed
uli
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SF
ab
ace
ae
Ing
ag
razi
ela
eB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MF
ab
ace
ae
Ing
ala
nce
ifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
S,
MF
ab
ace
ae
Ing
am
arg
ina
taB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SF
ab
ace
ae
Ing
asc
hin
ifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MF
ab
ace
ae
Ing
ase
ssil
isB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
SF
ab
ace
ae
Ing
ast
ria
taB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
Continuedonnextpage
16 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
RF
ab
ace
ae
Ing
asu
bn
ud
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SF
ab
ace
ae
Lo
nch
oca
rpu
scu
ltra
tus
Ab
ioti
cW
ind
NS
NS
Win
ged
MF
ab
ace
ae
Ma
cha
eriu
mb
rasi
lien
seA
bio
tic
Win
dN
SN
SW
ing
ed
MF
ab
ace
ae
Ma
cha
eriu
mn
yct
ita
ns
Ab
ioti
cW
ind
NS
NS
Win
ged
L,
SF
ab
ace
ae
My
roca
rpu
sfr
on
do
sus
Ab
ioti
cW
ind
NS
NS
Win
ged
R,
SF
ab
ace
ae
Orm
osi
aa
rbo
rea
Bio
tic
An
imal
En
do
zoo
cho
ryB
ird
Wit
ho
ut
rew
ard
SF
ab
ace
ae
Pip
tad
enia
pa
nic
ula
taA
bio
tic
Win
dN
SN
SD
ust
LF
ab
ace
ae
Pla
tym
isci
um
flo
rib
un
du
mA
bio
tic
Win
dN
SN
SW
ing
ed
SF
ab
ace
ae
Pse
ud
op
ipta
den
iale
pto
sta
chy
aA
bio
tic
Win
dN
SN
SW
ing
ed
S,
MF
ab
ace
ae
Pte
roca
rpu
sro
hri
iA
bio
tic
Win
dN
SN
SW
ing
ed
MF
ab
ace
ae
Sen
na
ma
cra
nth
era
Bio
tic
Sel
fB
aro
cho
ryN
SN
S
SF
ab
ace
ae
Sw
art
zia
lan
gsd
orf
fii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
R,
LF
ab
ace
ae
Sw
art
zia
sim
ple
xv
ar.
gra
nd
iflo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MF
ab
ace
ae
Sw
art
zia
sp.
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
R,
L,
SF
ab
ace
ae
Ta
chig
ali
den
ud
ata
Ab
ioti
cW
ind
NS
NS
Win
ged
SF
ab
ace
ae
Ta
chig
ali
mu
ltij
ug
aA
bio
tic
Win
dN
SN
SW
ing
ed
L,
SF
ab
ace
ae
Zo
lern
iail
icif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
SH
um
iria
cea
eH
um
iria
cea
esp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MH
um
iria
cea
eV
an
tan
eaco
mp
act
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SL
aci
stem
ace
ae
La
cist
ema
luci
du
mB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RL
aci
stem
ace
ae
La
cist
ema
pu
bes
cen
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
SL
am
iace
ae
Aeg
iph
ila
inte
gri
foli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
SL
am
iace
ae
Vit
excy
mo
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
ML
au
race
ae
An
iba
viri
dis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
ML
au
race
ae
Cin
na
mo
mu
mtr
ipli
ner
veB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
ML
au
race
ae
Cry
pto
cary
am
an
dio
cca
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
ML
au
race
ae
Cry
pto
cary
am
osc
ha
taB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
S,
ML
au
race
ae
Cry
pto
cary
asa
lig
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
ML
au
race
ae
Cry
pto
cary
asp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
R,
LL
au
race
ae
En
dli
cher
iap
an
icu
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
ML
au
race
ae
La
ura
cea
esp
.2
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
ML
au
race
ae
La
ura
cea
esp
.3
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
ML
au
race
ae
La
ura
cea
esp
.4
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
L,
S,
ML
au
race
ae
Lic
ari
aa
rmen
iaca
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SL
au
race
ae
Nec
tan
dra
nit
idu
laB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RL
au
race
ae
Nec
tan
dra
op
po
siti
foli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
ML
au
race
ae
Nec
tan
dra
psa
mm
op
hil
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SL
au
race
ae
Oco
tea
bey
rich
iiB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SL
au
race
ae
Oco
tea
bra
chy
bo
try
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
ML
au
race
ae
Oco
tea
cath
ari
nen
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
ML
au
race
ae
Oco
tea
da
ph
nif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
ML
au
race
ae
Oco
tea
dis
per
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
Continuedonnextpage
Biota Neotrop 17
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
L,
ML
au
race
ae
Oco
tea
gla
zio
vii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RL
au
race
ae
Oco
tea
rari
flo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
ML
au
race
ae
Oco
tea
silv
estr
isB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
ML
au
race
ae
Oco
tea
sp.
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SL
au
race
ae
Oco
tea
tab
aci
foli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LL
au
race
ae
Oco
tea
vell
ozi
an
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LL
au
race
ae
Rh
od
ost
emo
no
da
ph
ne
ma
cro
caly
xB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SL
ecy
thid
ace
ae
Ca
rin
ian
aes
trel
ensi
sA
bio
tic
Win
dN
SN
SW
ing
ed
LM
ag
no
lia
cea
eM
ag
no
lia
ova
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RM
alp
igh
iace
ae
By
rso
nim
ali
gu
stri
foli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
SM
alv
ace
ae
Eri
oth
eca
pen
taphyll
aA
bio
tic
Win
dN
SN
SP
lum
ed
L,
SM
alv
ace
ae
Qu
ara
rib
eatu
rbin
ata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MM
ela
sto
ma
tace
ae
Mel
ast
om
ata
cea
esp
.N
IN
IN
IN
IN
I
SM
ela
sto
ma
tace
ae
Mer
ian
iaca
lyp
tra
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Ba
cco
id
MM
ela
sto
ma
tace
ae
Mic
on
iaca
bu
ssu
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
RM
ela
sto
ma
tace
ae
Mic
on
iaci
nn
am
om
ifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
RM
ela
sto
ma
tace
ae
Mic
on
iad
od
eca
nd
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Ba
cco
id
R,
LM
ela
sto
ma
tace
ae
Mic
on
iap
rasi
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
RM
ela
sto
ma
tace
ae
Mic
on
iap
usi
llif
lora
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
S,
MM
ela
sto
ma
tace
ae
Mic
on
iasp
.1
(new
spec
ies)
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
MM
ela
sto
ma
tace
ae
Mic
on
iasp
.2
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
SM
ela
sto
ma
tace
ae
Mic
on
iatr
isti
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Ba
cco
id
MM
ela
sto
ma
tace
ae
Mic
on
iava
lth
eri
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
R,
MM
ela
sto
ma
tace
ae
Tib
ou
chin
ap
ulc
hra
Ab
ioti
cW
ind
NS
NS
Du
st
MM
ela
sto
ma
tace
ae
Tib
ou
chin
asp
.A
bio
tic
Win
dN
SN
SD
ust
L,
S,
MM
elia
cea
eC
ab
rale
aca
nje
ran
asu
bsp
.ca
nje
ran
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
S,
MM
elia
cea
eC
edre
lao
do
rata
Ab
ioti
cW
ind
NS
NS
Win
ged
MM
elia
cea
eG
ua
rea
ku
thia
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
L,
S,
MM
elia
cea
eG
ua
rea
ma
cro
ph
yll
asu
bsp
.tu
ber
cu-
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
L,
S,
MM
elia
cea
eT
rich
ilia
silv
ati
caB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
MM
emec
yla
cea
eM
ou
riri
cha
mis
soa
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
MM
on
imia
cea
eM
oll
ined
iaa
rgy
rog
yn
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SM
on
imia
cea
eM
oll
ined
iab
ora
cen
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
on
imia
cea
eM
oll
ined
iael
ega
ns
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
on
imia
cea
eM
oll
ined
iaen
gle
ria
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
on
imia
cea
eM
oll
ined
iag
lab
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LM
on
imia
cea
eM
oll
ined
iala
mp
rop
hy
lla
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
on
imia
cea
eM
oll
ined
iao
vata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
S,
MM
on
imia
cea
eM
oll
ined
iasc
ho
ttia
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
S,
MM
on
imia
cea
eM
oll
ined
iasp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
LM
on
imia
cea
eM
oll
ined
iatr
iflo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
Continuedonnextpage
18 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
L,
SM
ora
cea
eB
rosi
mu
mg
uia
nen
seB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
LM
ora
cea
eB
rosi
mu
mla
ctes
cen
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SM
ora
cea
eF
icu
scf
.h
irsu
taB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
LM
ora
cea
eF
icu
sg
lab
raB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
R,
LM
ora
cea
eF
icu
sin
sip
ida
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
LM
ora
cea
eF
icu
sp
ulc
hel
laB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
MM
ora
cea
eF
icu
ssp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
L,
SM
ora
cea
eS
oro
cea
bo
np
lan
dii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
L,
SM
ora
cea
eS
oro
cea
hil
ari
iB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
RM
ora
cea
eS
oro
cea
jure
ian
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
R,
L,
SM
yri
stic
ace
ae
Vir
ola
bic
hu
yb
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
SM
yri
stic
ace
ae
Vir
ola
ga
rdn
eri
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
RM
yrt
ace
ae
Ca
lyp
tra
nth
esco
nci
nn
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
S,
MM
yrt
ace
ae
Ca
lyp
tra
nth
eslu
cid
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MM
yrt
ace
ae
Ca
lyp
tra
nth
esru
faB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MM
yrt
ace
ae
Ca
lyp
tra
nth
essp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
S,
MM
yrt
ace
ae
Ca
lyp
tra
nth
esst
rig
ipes
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
R,
L,
S,
MM
yrt
ace
ae
Ca
mp
om
an
esia
gu
avi
rob
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Ba
cco
id
L,
SM
yrt
ace
ae
Ca
mp
om
an
esia
lau
rifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dB
acc
oid
RM
yrt
ace
ae
Eu
gen
iaa
stri
ng
ens
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Eu
gen
iab
ati
ng
ab
ran
caB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
Eu
gen
iab
rasi
lien
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SM
yrt
ace
ae
Eu
gen
iab
revi
sty
laB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MM
yrt
ace
ae
Eu
gen
iab
urk
art
ian
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MM
yrt
ace
ae
Eu
gen
iace
rasi
flo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LM
yrt
ace
ae
Eu
gen
iace
reja
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SM
yrt
ace
ae
Eu
gen
iacf
.fl
am
ing
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
S,
MM
yrt
ace
ae
Eu
gen
iacu
pre
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SM
yrt
ace
ae
Eu
gen
iaex
cels
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
SM
yrt
ace
ae
Eu
gen
iafu
sca
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RM
yrt
ace
ae
Eu
gen
iah
an
dro
an
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LM
yrt
ace
ae
Eu
gen
iam
ag
nib
ract
eola
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
SM
yrt
ace
ae
Eu
gen
iam
on
osp
erm
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MM
yrt
ace
ae
Eu
gen
iao
blo
ga
nta
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Eu
gen
iap
isif
orm
isB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LM
yrt
ace
ae
Eu
gen
iap
lica
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MM
yrt
ace
ae
Eu
gen
iap
rasi
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SM
yrt
ace
ae
Eu
gen
iap
run
ifo
rmis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Eu
gen
iasp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
LM
yrt
ace
ae
Eu
gen
iasp
.3
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Eu
gen
iasp
.4
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
Continuedonnextpage
Biota Neotrop 19
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
MM
yrt
ace
ae
Eu
gen
iasp
.5
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Eu
gen
iasp
.1
3B
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
Eu
gen
iasp
ecio
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SM
yrt
ace
ae
Eu
gen
iasu
ba
ven
iaB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SM
yrt
ace
ae
Eu
gen
iate
rna
tifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SM
yrt
ace
ae
Eu
gen
iave
rtic
ila
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
Eu
gen
iave
rtic
illa
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SM
yrt
ace
ae
Ma
rlie
rea
gla
zio
via
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
R,
LM
yrt
ace
ae
Ma
rlie
rea
ob
scu
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SM
yrt
ace
ae
Ma
rlie
rea
race
mo
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
S,
MM
yrt
ace
ae
Ma
rlie
rea
silv
ati
caB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
S,
MM
yrt
ace
ae
Ma
rlie
rea
tom
ento
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SM
yrt
ace
ae
My
rceu
gen
iaca
mp
estr
isB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
S,
MM
yrt
ace
ae
My
rceu
gen
iam
yrc
ioid
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SM
yrt
ace
ae
My
rcia
aet
hu
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
My
rcia
bra
sili
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MM
yrt
ace
ae
My
rcia
gu
ian
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
My
rcia
insu
lare
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
My
rcia
mu
ltif
lora
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SM
yrt
ace
ae
My
rcia
neo
bla
nch
etia
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RM
yrt
ace
ae
My
rcia
pu
bip
eta
laB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
RM
yrt
ace
ae
My
rcia
race
mo
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MM
yrt
ace
ae
My
rcia
spec
tab
ilis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
R,
MM
yrt
ace
ae
My
rcia
sple
nd
ens
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
S,
MM
yrt
ace
ae
My
rcia
ria
flo
rib
un
da
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
My
rta
cea
esp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
RM
yrt
ace
ae
My
rta
cea
esp
.2
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
MM
yrt
ace
ae
My
rta
cea
esp
.3
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
MM
yrt
ace
ae
My
rta
cea
esp
.9
Bio
tic
An
ima
lE
nd
ozo
och
ory
NI
NI
MM
yrt
ace
ae
My
rta
cea
esp
.1
0B
ioti
cA
nim
al
En
do
zoo
cho
ryN
IN
I
SM
yrt
ace
ae
Neo
mit
ran
thes
glo
mer
ata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MM
yrt
ace
ae
Pim
enta
pse
ud
oca
ryo
ph
yll
us
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
LM
yrt
ace
ae
Pli
nia
com
pla
na
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SM
yrt
ace
ae
Pli
nia
edu
lis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
RM
yrt
ace
ae
Sy
zyg
ium
jam
bo
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MN
yct
ag
ina
cea
eG
ua
pir
aa
reo
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SN
yct
ag
ina
cea
eG
ua
pir
ah
irsu
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
S,
MN
yct
ag
ina
cea
eG
ua
pir
an
itid
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
S,
MN
yct
ag
ina
cea
eG
ua
pir
ao
pp
osi
taB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SO
chn
ace
ae
Ou
rate
ap
arv
iflo
raB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MO
laca
cea
eH
eist
eria
silv
ian
iiB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SO
laca
cea
eT
etra
sty
lid
ium
gra
nd
ifo
liu
mB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
Continuedonnextpage
20 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
MO
pil
iace
ae
Ag
on
an
dra
exce
lsa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
R,
L,
S,
MP
hyll
an
thace
ae
Hie
ron
ym
aa
lch
orn
eoid
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MP
iper
ace
ae
Pip
erce
rnu
um
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
RP
oly
go
na
cea
eC
occ
olo
ba
gla
zio
vii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RP
rim
ula
cea
eM
yrs
ine
cori
ace
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
MP
rim
ula
cea
eM
yrs
ine
ga
rdn
eria
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
S,
MP
rim
ula
cea
eM
yrs
ine
her
mo
gen
esii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RP
rim
ula
cea
eM
yrs
ine
ven
osa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SP
rim
ula
cea
eS
tylo
gy
ne
lho
tsk
ya
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RP
rote
ace
ae
Eu
pla
ssa
can
tare
ira
eB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MP
rote
ace
ae
Eu
pla
ssa
ho
ehn
eiB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
R,
LP
rote
ace
ae
Ro
up
ala
mo
nta
na
va
r.b
rasi
lien
sis
Ab
ioti
cW
ind
NS
NS
Win
ged
MQ
uii
na
cea
eQ
uii
na
aff
.m
ag
all
an
o-g
om
esii
(new
spec
ies)
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
R,
SR
osa
cea
eP
run
us
my
rtif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SR
ub
iace
ae
Als
eis
flo
rib
un
da
Ab
ioti
cW
ind
NS
NS
Du
st
RR
ub
iace
ae
Am
aio
ua
inte
rmed
iaB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
S,
MR
ub
iace
ae
Ba
thy
saa
ust
rali
sA
bio
tic
Win
dN
SN
SD
ust
L,
SR
ub
iace
ae
Ba
thy
sam
end
on
caei
Ab
ioti
cW
ind
NS
NS
Du
st
SR
ub
iace
ae
Ba
thy
sast
ipu
lata
Ab
ioti
cW
ind
NS
NS
Du
st
MR
ub
iace
ae
Ch
om
elia
ped
un
culo
saB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SR
ub
iace
ae
Co
uss
are
aa
cced
ens
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
SR
ub
iace
ae
Co
uss
are
am
erid
ion
ali
sv
ar.
po
rop
hy
laB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
R,
L,
SR
ub
iace
ae
Fa
ram
eap
ach
ya
nth
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LR
ub
iace
ae
Fara
mea
pic
inguabae
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
RR
ub
iace
ae
Gen
ipa
infu
nd
ibu
lifo
rmis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
L,
SR
ub
iace
ae
Ixo
rab
ract
eola
ris
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
L,
S,
MR
ub
iace
ae
Po
soq
uer
iala
tifo
lia
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
SR
ub
iace
ae
Psy
cho
tria
bir
otu
laB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MR
ub
iace
ae
Psy
cho
tria
lon
gip
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SR
ub
iace
ae
Psy
cho
tria
ma
po
uri
oid
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SR
ub
iace
ae
Psy
cho
tria
nu
da
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
SR
ub
iace
ae
Psy
cho
tria
pa
ten
tin
ervi
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
MR
ub
iace
ae
Psy
cho
tria
vell
osi
an
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
MR
ub
iace
ae
Ru
bia
cea
esp
.1
NI
NI
NI
NI
NI
LR
ub
iace
ae
Ru
dg
eaco
ron
ata
sub
sp.
leio
carp
oid
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
SR
ub
iace
ae
Ru
dg
eaja
smin
oid
esB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
L,
SR
ub
iace
ae
Ru
dg
eave
ller
eaB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
LR
ub
iace
ae
Ru
stia
form
osa
Ab
ioti
cW
ind
NS
NS
Win
ged
LR
ub
iace
ae
Sim
ira
sam
pa
ioa
na
Ab
ioti
cW
ind
NS
NS
Win
ged
LR
ub
iace
ae
Sim
ira
viri
dif
lora
Ab
ioti
cW
ind
NS
NS
Win
ged
Continuedonnextpage
Biota Neotrop 21
Dispersal spectrum at the Atlantic Rainforest
http://dx.doi.org/10.1590/S1676-06032014000313 http://www.scielo.br/bn
., 14(1): e20130003, 2014
Tab
le.
Co
nti
nu
ed.
Fo
rest
typ
eF
am
ily
Gen
era
Sp
ecie
sL
evel
1L
evel
2L
evel
3L
evel
4L
evel
5
MR
uta
cea
eR
uta
cea
esp
.N
IN
IN
IN
IN
I
LR
uta
cea
eZ
an
tho
xy
lum
fag
ara
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MS
ab
iace
ae
Mel
iosm
ase
llo
wii
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
MS
ali
cace
ae
Ca
sea
ria
ob
liq
ua
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
MS
ali
cace
ae
Ca
sea
ria
pa
ran
aen
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
S,
MS
ali
cace
ae
Ca
sea
ria
sylv
estr
isB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
SS
ap
ind
ace
ae
All
op
hy
llu
sp
etio
latu
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Dru
po
id
S,
MS
ap
ind
ace
ae
Cu
pa
nia
furf
ura
cea
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
R,
L,
S,
MS
ap
ind
ace
ae
Cu
pa
nia
ob
lon
gif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
MS
ap
ind
ace
ae
Cu
pa
nia
vern
ali
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
RS
ap
ind
ace
ae
Ma
tay
ba
ela
eag
no
ides
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dF
lesh
ya
pp
end
ag
e
MS
ap
ind
ace
ae
Ma
tay
ba
gu
ian
ensi
sB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
SS
ap
ind
ace
ae
Ma
tay
ba
jug
lan
dif
oli
aB
ioti
cA
nim
al
En
do
zoo
cho
ryB
ird
Fle
shy
ap
pen
da
ge
L,
SS
ap
ota
cea
eC
hry
sop
hy
llu
mfl
exu
osu
mB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
MS
ap
ota
cea
eC
hry
sop
hy
llu
min
orn
atu
mB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
MS
ap
ota
cea
eC
hry
sop
hy
llu
mvi
rid
eB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
L,
S,
MS
ap
ota
cea
eE
ccli
nu
sara
mif
lora
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
SS
ap
ota
cea
eM
icro
ph
oli
scr
ass
iped
icel
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MS
ap
ota
cea
eM
icro
ph
oli
sg
ard
ner
ian
aB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
S,
MS
ap
ota
cea
eP
ou
teri
aca
imit
oB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
S,
MS
ap
ota
cea
eP
ou
teri
ag
ard
ner
iB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
LS
ap
ota
cea
eP
ou
teri
ap
sam
mo
ph
ila
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
L,
SS
ap
ota
cea
eP
ou
teri
ave
no
saB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
SS
ap
ota
cea
eP
rad
osi
ala
ctes
cen
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lA
ttra
ctiv
eco
lou
rs
LS
ap
ota
cea
eS
ap
ota
cea
esp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
LS
ap
ota
cea
eS
ap
ota
cea
esp
.2
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
SS
ap
ota
cea
eS
ap
ota
cea
esp
.3
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Att
ract
ive
colo
urs
MS
ola
na
cea
eA
ure
lia
na
fasc
icu
lata
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
LS
ola
na
cea
eS
ola
na
cea
esp
.B
ioti
cA
nim
al
En
do
zoo
cho
ryN
IN
I
MS
ola
na
cea
eS
ola
nu
ma
ff.
refe
scen
sB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
MS
ola
na
cea
eS
ola
nu
mci
nn
am
om
um
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
MS
ola
na
cea
eS
ola
nu
mp
seu
do
qu
ina
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
MS
ola
na
cea
eS
ola
nu
msp
.1
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
MS
ola
na
cea
eS
ola
nu
msw
art
izia
nu
mB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
MS
ola
na
cea
eS
ola
nu
mve
llo
zia
nu
mB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
S,
MT
hy
mel
aea
cea
eD
ap
hn
op
sis
sch
wa
ckea
na
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
MU
nd
eter
min
edU
nd
eter
min
edsp
.8
NI
NI
NI
NI
NI
MU
nd
eter
min
edU
nd
eter
min
edsp
.9
NI
NI
NI
NI
NI
R,
L,
S,
MU
rtic
ace
ae
Cec
rop
iag
lazi
ovi
iB
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
R,
L,
S,
MU
rtic
ace
ae
Co
uss
ap
oa
mic
roca
rpa
Bio
tic
An
ima
lE
nd
ozo
och
ory
Ma
mm
al
Cle
ar
an
do
pa
qu
e
MU
rtic
ace
ae
Co
uss
ap
oa
sp.
1B
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
MU
rtic
ace
ae
Co
uss
ap
oa
sp.
2B
ioti
cA
nim
al
En
do
zoo
cho
ryM
am
ma
lC
lea
ra
nd
op
aq
ue
L,
SU
rtic
ace
ae
Po
uro
um
ag
uia
nen
sis
Bio
tic
An
ima
lE
nd
ozo
och
ory
Bir
dD
rup
oid
22 Biota Neotrop
Martins, V.F. et al.
http://www.scielo.br/bn http://dx.doi.org/10.1590/S1676-06032014000313
., 14(1): e20130003, 2014